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Invited review: Review of taxonomic changes in dairy-related lactobacilli

Open AccessPublished:February 24, 2022DOI:https://doi.org/10.3168/jds.2021-21138

      ABSTRACT

      The genus Lactobacillus has represented an extremely large and diverse collection of bacteria that populate a wide range of habitats, and which may have industrial applications. Researchers have grappled with the immense genetic, metabolic, and ecological diversity within the genus Lactobacillus for many years. As a result, the taxonomy of lactobacilli has been extensively revised, incorporating new genus names for many lactobacilli based on their characteristics including genomic similarities. As a result, many lactobacilli traditionally associated with dairy products now have new genus names and are grouped into new clades or clusters of species. In this review, we examine how the taxonomic restructuring of the genus Lactobacillus will affect the dairy industry and discuss lactobacilli associated with dairy production, processing, and those that confer possible health benefits when delivered by dairy products.

      Key words

      INTRODUCTION

      What is in a name? Taxonomy is the science of systematically classifying organisms into a hierarchy (domain, phylum, class, order, family, genus, species, subspecies) based on characteristics that indicate relatedness. Taxonomically, organisms more closely related share more genetic similarities, and, hence, more phenotypic traits in common. Biologists use taxonomy as the basis for nomenclature, or naming of organisms. Biological nomenclature is important so that there can be common and consistent communication about living organisms for scientific research or medical and industrial applications (
      • Parker C.T.
      • Tindall B.J.
      • Garrity G.M.
      International Code of Nomenclature of Prokaryotes.
      ).
      For microorganisms, taxonomic classification can be difficult because they lack many obvious distinguishing features, and due to horizontal gene transfer, distantly related organisms may share similar physiologic characteristics. New genetic methods, especially whole genome sequencing, provide more precise metrics for defining microbial taxonomy. This allows researchers to capture an organism's physiological, ecological, and evolutionary relationship more accurately. The genus name Lactobacillus has represented an extremely large and diverse collection of microorganisms that inhabit a wide range of habitats, and many may have industrial and medical applications. Because of the genetic and ecological diversity within the genus Lactobacillus,
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      have recently reevaluated the genus and provided new genus names that group organisms into new clades or clusters of species. This includes the lactobacilli that are common in dairy foods and products. The purpose of this review is to help dairy producers and dairy researchers who do not have a strong microbiology background understand the taxonomic restructuring of the Lactobacillus genus. The organisms discussed are primarily the lactobacilli associated with dairy production, processing, and those that confer possible health benefits when delivered by dairy products.

      INITIAL LACTOBACILLUS TAXONOMY

      Researchers have been grappling with the immense genetic, metabolic, and ecological diversity within the genus Lactobacillus for many years (
      • Vandamme P.
      • Pot B.
      • Gillis M.
      • De Vos P.
      • Kersters K.
      • Swings J.
      Polyphasic taxonomy, a consensus approach to bacterial systematics.
      ;
      • Felis G.E.
      • Dellaglio F.
      Taxonomy of Lactobacilli and Bifidobacteria.
      ;
      • Salvetti E.
      • Torriani S.
      • Felis G.E.
      The genus Lactobacillus: A taxonomic update.
      ;
      • Mattarelli P.
      • Holzapfel W.
      • Franz C.
      • Endo A.
      • Felis G.E.
      • Hammes W.
      • Pot B.
      • Dicks L.
      • Dellaglio F.
      Recommended minimal standards for description of new taxa of the genera Bifidobacterium, Lactobacillus and related genera.
      ;
      • Zheng J.
      • Ruan L.
      • Sun M.
      • Gänzle M.
      A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology.
      ;
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Wittouck S.
      • Wuyts S.
      • Lebeer S.
      Towards a genome-based reclassification of the genus Lactobacillus..
      ,
      • Wittouck S.
      • Wuyts S.
      • Meehan C.J.
      • van Noort V.
      • Lebeer S.
      A genome-based species taxonomy of the Lactobacillus genus complex.
      ;
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Lactobacilli were some of the earliest bacteria described due, in part, to their presence in the microbiota of fermented milks and their reported health benefits to consumers (
      • Tannock G.W.
      A special fondness for lactobacilli.
      ). Initially, taxonomy of microorganisms (bacteria) was based on their physical characteristics (gram strain, cell morphology, colony appearance) and on their growth parameters such as optimum incubation temperature, pH tolerance, and oxygen requirements. Methods based on specific composition of cell components were also used to differentiate lactobacilli including cell wall (peptidoglycan) composition and membrane fatty acid profiles (
      • Davis G.H.G.
      Notes on the phylogenetic background to Lactobacillus taxonomy.
      ). These classifications are only as accurate as the databases used for comparison and, in the case of cell membrane composition, also dependent on the growth media because it can influence fatty acid composition.
      Biochemical characterization, determining substrates utilized and the metabolic end products produced, generated a phenotype-based taxonomy for lactobacilli. This was used to divide lactobacilli into 3 general groups based on their fermentative ability; obligate homofermenters, facultative heterofermenters, and obligate heterofermenters (
      • Hammes W.P.
      • Vogel R.F.
      The genus Lactobacillus..
      ). These designations (classifications) were based on lactobacilli either having or lacking key enzymes in several fermentation pathways. Obligate homofermenters use the Embden-Meyerhof pathway to convert glucose to lactic acid, but cannot use the pentose phosphate pathway to ferment pentoses. Obligate heterofermenters exclusively use the pentose phosphate pathway, whereas facultative heterofermenters using the Embden-Meyerhof pathway but also ferment pentoses. This classification proved very useful in dairy production because lactobacilli from each category play significant roles in dairy processing and product quality.
      In the 1980s, bacterial taxonomy entered the genetic age with the use of DNA sequencing to determine the 16S rRNA gene base sequence. Comparison of 16S rRNA gene base sequences allowed the generation of a true phylogenetic tree for taxonomy, which graphed the relatedness of lactobacilli based on divergence from common ancestors. It quickly became the gold standard for determining the place of an organism on the taxonomic tree and gave accurate genus and species designations because metabolic properties among lactobacilli were more variable than initially thought (
      • Williams A.G.
      • Withers S.E.
      • Banks J.M.
      Energy sources of non-starter lactic acid bacteria isolated from Cheddar cheese.
      ;
      • Clarridge III, J.E.
      Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases.
      ).

      Revised Taxonomy for Lactobacillus

      Development of whole genome sequencing, and the computational capacity to rapidly compare entire bacterial genomes, dramatically advanced bacterial taxonomy. Recent studies utilizing this approach, culminating in
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      , proposed using a variety of genomics metrics for classifying organisms within the Lactobacillus genus and argued for a revision to its taxonomy (
      • Mattarelli P.
      • Holzapfel W.
      • Franz C.
      • Endo A.
      • Felis G.E.
      • Hammes W.
      • Pot B.
      • Dicks L.
      • Dellaglio F.
      Recommended minimal standards for description of new taxa of the genera Bifidobacterium, Lactobacillus and related genera.
      ;
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Salvetti E.
      • Harris H.
      • Felis G.E.
      • O'Toole P.W.
      Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification.
      ;
      • Wittouck S.
      • Wuyts S.
      • Meehan C.J.
      • van Noort V.
      • Lebeer S.
      A genome-based species taxonomy of the Lactobacillus genus complex.
      ;
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). The ability to sequence an organism's genome and to compare the sequence of key conserved proteins between genomes has allowed restructuring of Lactobacillus taxonomy and the clarification of taxonomic relationships based on genetic, physiological, and ecological characteristics. Although original Lactobacillus taxonomies were based on their ability to ferment specific hexoses, that classification has been superseded by genomic analysis which showed that metabolic capabilities were not sufficient for representing the diversity or evolutionary history of this group. Species within this taxon share only a small number of core genes, whereas the pan genome (the entire collection of genes within the genus) of the Lactobacillus genus complex is very large (
      • Broadbent J.R.
      • Neeno-Eckwall E.C.
      • Stahl B.
      • Tandee K.
      • Cai H.
      • Morovic W.
      • Horvath P.
      • Heidenreich J.
      • Perna N.T.
      • Barrangou R.
      • Steele J.L.
      Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation.
      ;
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Wittouck S.
      • Wuyts S.
      • Meehan C.J.
      • van Noort V.
      • Lebeer S.
      A genome-based species taxonomy of the Lactobacillus genus complex.
      ). This diversity is attributed to adaptations to diverse environments and horizontal gene transfer events through mobile elements and bacteriophage (
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Stefanovic E.
      • Fitzgerald G.
      • McAuliffe O.
      Advances in the genomics and metabolomics of dairy lactobacilli: A review.
      ;
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ).
      The amount of genetic diversity calculated based on total nucleotide identity, average nucleotide identity, GC content, genome size, and pan genome comparisons support the conclusion that diversity within the former genus Lactobacillus was at least equivalent to that seen within biological families (
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Zheng J.
      • Ruan L.
      • Sun M.
      • Gänzle M.
      A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology.
      ). Further, the former genus Lactobacillus is paraphyletic with the family Leuconostocaceae and genus Pediococcus, indicating evolutionary relationships within these taxa were not adequately resolved and that a revised taxonomy was necessary to meet the standard expectations for defined genera (
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      ;
      • Salvetti E.
      • Harris H.
      • Felis G.E.
      • O'Toole P.W.
      Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification.
      ;
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). Recently, an analysis of over 2,400 Lactobacillus genomes examined Lactobacillus taxonomy using a 6% difference for speciation to suggest restructuring the taxonomy into 239 de novo species and 8 new species (
      • Wittouck S.
      • Wuyts S.
      • Lebeer S.
      Towards a genome-based reclassification of the genus Lactobacillus..
      ,
      • Wittouck S.
      • Wuyts S.
      • Meehan C.J.
      • van Noort V.
      • Lebeer S.
      A genome-based species taxonomy of the Lactobacillus genus complex.
      ). The number of Lactobacillus species, which exceeded 260 (Table 1), has proven cumbersome with some species in groups not representative of their metabolic characteristics, natural environment, or common genetic sequences. Modern sequencing technology and bioinformatic analysis, combined with new information about physiology, habitat, and lifestyle, have made a more robust classification of the lactobacilli possible (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ).
      Table 1Number of lactobacilli species over time
      YearNumber of speciesReference
      199567
      • Hammes W.P.
      • Vogel R.F.
      The genus Lactobacillus..
      200380
      • Satokari R.M.
      • Vaughan E.E.
      • Smidt H.
      • Saarela M.
      • Mättö J.
      • de Vos W.M.
      Molecular approaches for the detection and identification of bifidobacteria and lactobacilli in the human gastrointestinal tract.
      2007106
      • Felis G.E.
      • Dellaglio F.
      Taxonomy of Lactobacilli and Bifidobacteria.
      2012152
      • Salvetti E.
      • Torriani S.
      • Felis G.E.
      The genus Lactobacillus: A taxonomic update.
      2015213
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      2020261
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      used a polyphasic approach to characterize 261 described species of Lactobacillus, Pediococcus, and Leuconostocaceae. A polyphasic approach involves comparisons of genomic analysis, phenotypic characteristics, and ecological habitats. Genetic metrics used included average nucleotide identity, average AA identity, core-gene AA identity, and conserved genes. This analysis divided the genus Lactobacillus into 26 lineages with 23 new genera, which captured the evolutionary lineage of Lactobacillaceae, and can serve as a useful and practical taxonomy (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ).
      Several metabolic and genetic trends become more apparent in the updated taxonomy. The heterofermentative and homofermentative species of lactobacilli generally separate into 2 large groups within the family Lactobacillaceae. The terms obligate and facultative are no longer used in the description of fermentation. The new definition of homofermentative organisms is those that metabolize hexoses using the Embden-Meyerhoff pathway to pyruvate, and heterofermentative organisms are those that metabolize hexoses using the phosphoketolase pathway to pyruvate and acetyl-phosphate. Pentose metabolism is still considered variable across the new taxonomic groups at the species and strain level and is not used as a defining feature. Within each group, other characteristics are also consistent within the phylogenomic classification and proposed genera, including metabolic similarities, signature genes, and similar habitats (
      • Zheng J.
      • Ruan L.
      • Sun M.
      • Gänzle M.
      A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology.
      ;
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ;
      • Salvetti E.
      • Harris H.
      • Felis G.E.
      • O'Toole P.W.
      Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification.
      ;
      • Wittouck S.
      • Wuyts S.
      • Lebeer S.
      Towards a genome-based reclassification of the genus Lactobacillus..
      ;
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). For example, lactobacilli symbiotic with humans or mammals have a decreased genome size, but retain a large carbohydrate range, presumably as an adaptation to diets containing diverse substrates. These symbionts may also show acid or bile resistance (
      • Zheng J.
      • Ruan L.
      • Sun M.
      • Gänzle M.
      A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology.
      ;
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ). In comparison, most lactobacilli involved with food fermentations, including dairy, have larger genomes that may provide habitat flexibility and are considered either free-living or nomadic, meaning they are found in diverse habitats or have a prime habitat that has not been identified (
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ;
      • Stefanovic E.
      • Thierry A.
      • Maillard M.
      • Bertuzzi A.
      • Rea M.C.
      • Fitzgerald G.
      • McAuliffe O.
      • Kilcawley K.N.
      Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems.
      ).
      Lactobacilli used in food fermentations do not cluster in distinct genera in the new taxonomy, but instead are found throughout the Lactobacillaceae suggesting that they have a free-living ancestor associated with either animals or plants (
      • Stefanovic E.
      • Fitzgerald G.
      • McAuliffe O.
      Advances in the genomics and metabolomics of dairy lactobacilli: A review.
      ). Most members of Paucilactobacillus for example, have been isolated from silage or plant-related environments, but they have also been found in dairy products, sometimes as defect-causing contaminants (
      • Oberg C.J.
      • Oberg T.S.
      • Culumber M.D.
      • Ortakci F.
      • Broadbent J.R.
      • McMahon D.J.
      Lactobacillus wasatchensis sp. nov., a non-starter lactic acid bacteria isolated from aged Cheddar cheese.
      ). Other physiological traits that appear to cluster in phylogroups and that may have applications to dairy include acid resistance, bacteriocin production, bacteriophage resistance, carbohydrate use patterns, lactate metabolism, and amino acid metabolism pathways (
      • Zheng J.
      • Ruan L.
      • Sun M.
      • Gänzle M.
      A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology.
      ,
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ).

      Need for Reclassification in the Dairy Industry

      The economic applications of the Lactobacillaceae in food, probiotic, industrial, and medical applications complicate the argument for reclassification because the genus name Lactobacillus is ubiquitous and familiar. However, reclassification is important because the applications of lactobacilli in industry depends on the use of species or strains with the desired metabolic capabilities and growth parameters (
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ;
      • Stefanovic E.
      • Thierry A.
      • Maillard M.
      • Bertuzzi A.
      • Rea M.C.
      • Fitzgerald G.
      • McAuliffe O.
      • Kilcawley K.N.
      Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems.
      ;
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). The phylogenomic taxonomy developed by
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      is largely consistent with metabolic capabilities, lifestyle strategies, and habitats. The new taxonomy will be of greater value for industrial and medical applications (
      • Duar R.M.
      • Lin X.B.
      • Zheng J.
      • Martino M.E.
      • Grenier T.
      • Pérez-Muñoz M.E.
      • Leulier F.
      • Gänzle M.
      • Walter J.
      Lifestyles in transition: evolution and natural history of the genus Lactobacillus..
      ;
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ), because it will be easier to identify specific organisms that have the desired metabolic pathways, products, and growth conditions required for commercial or medical production.
      This is especially important in dairy because an organism's ability to produce a desired product requires strictly defined, and reproducible, growth parameters such as the types and amount of sugars, fermentation temperatures, and presence of other organisms. Even within the dairy industry, lactobacilli occur in diverse habitats or ecosystems and have a wide variety of roles and effects (
      • Stefanovic E.
      • Thierry A.
      • Maillard M.
      • Bertuzzi A.
      • Rea M.C.
      • Fitzgerald G.
      • McAuliffe O.
      • Kilcawley K.N.
      Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems.
      ). The reclassification by
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      allows improved communication among scientists, industries, regulators, and the public about the specific capabilities of each species (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). It will also allow for greater consistency and reproducibility, especially in the food industry, and potentially can be used to identify genes for creating designer lactobacilli that precisely deliver a desired product (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). A higher resolution framework based on physiological and ecological characteristics, in addition to genomic similarities, will help those in industry identify organisms more likely to meet application demands, produce desired products, or identify ways for controlling unwanted organisms without inhibiting those that have desired capabilities.
      The taxonomic revision will require dramatic and potentially expensive changes for the scientific community, companies, governments, and, even, consumers. Long-term stability of the new nomenclature is of the utmost importance, so that newly identified organisms can be absorbed into the taxonomy in a meaningful way. This is especially important as new organisms are now being discovered, often without cultured representatives, through next-generation sequencing of complex environments such as the microbiome of the gut (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ).
      Revision of Lactobacillus nomenclature is not without concern or controversy. Reclassification may initially cause problems because of regulatory, safety, or legal complications and misunderstandings (
      • Salvetti E.
      • Harris H.
      • Felis G.E.
      • O'Toole P.W.
      Comparative genomics of the genus Lactobacillus reveals robust phylogroups that provide the basis for reclassification.
      ;
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ;
      • Wittouck S.
      • Wuyts S.
      • Meehan C.J.
      • van Noort V.
      • Lebeer S.
      A genome-based species taxonomy of the Lactobacillus genus complex.
      ). A stable nomenclature is necessary for clear communication between stakeholders. Commercial and legal effects of the taxonomic change include patent applications and enforcement, ingredient lists, import and export certifications, marketing, and consumer education (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). Realizing implementation of name changes may take a substantial amount of time, but as noted at a workshop of the Lactic Acid Bacteria Industrial Platform, efforts to communicate the change through an easy-to-use website or cell phone app would help facilitate the change (
      • Pot B.
      • Salvetti E.
      • Mattarelli P.
      • Felis G.E.
      The potential impact of the Lactobacillus name change: The results of an expert meeting organized by the Lactic Acid Bacteria Industrial Platform (LABIP).
      ). Such a website exists at http://lactobacillus.ualberta.ca/ where old names of Lactobacillus species can be entered, and the new genus names and descriptions are provided.
      Lactobacilli relevant to the dairy industry have been organized into categories based on relevance to the industry with their original taxonomic name and new taxonomic designation (Table 2). In addition, supplemental material has been added relative to each organism's role in dairy microbiology. If an organism has multiple uses or roles in dairy microbiology, it is grouped with its most significant role and additional roles are added in the description. Tables have been used to assist in finding organisms in functional groupings and for listing the new taxonomic names of lactobacilli with minor connections to the dairy industry. The 16S rRNA gene accession number, genome size including G+C content, genome sequence accession number and the culture repository for each organism described in this review can be found in
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      . In addition,
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      also contains the reference to the original description of each species when it was initially proposed along with the basonym, which is the original proposed species name and the author citation, and the type strain.
      Table 2Abbreviations for dairy-related Lactobacilli
      GenusAbbreviationSpecies; common source
      Lactobacillus
      Homofermentative.
      Lb.delbrueckii
      Species are the type species for this genus.
      delbrueckii ssp. bulgaricus; yogurt, cheese delbrueckii ssp. lactis; milk, cheese delbrueckii ssp. indicus; fermented dairy product (dahi) helveticus; sour milk, cheese, silage acidophilus; no mention of isolation from dairy products other than use as starter. kefiranofaciens ssp. kefirgranum; kefir grains, sour milk kefiranofaciens ssp. kefiranofaciens; -kefir grains and other fermented dairy products acetotolerans; silage helsingborgensis; alfalfa silage taiwanensis; silage amylovorus; cattle waste-cord fermentation
      Lacticaseibacillus
      Homofermentative.
      Lcb.casei
      Species are the type species for this genus.
      ; silage, most previous designations should be reclassified as paracasei paracasei paracasei ssp. paracasei; dairy products and silage paracasei ssp. tolerans; dairy products rhamnosus; dairy products nasuensis; grass silage chiayiensis; cow manure
      Lactiplantibacillus
      Homofermentative.
      Lpb.plantarum; dairy fermentations plantarum ssp. plantarum; dairy products and dairy environments, cow dung, silage plantarum ssp. argentoratensis; elephant grass silage paraplantarum; dairy products, sow milk, silage pentosus; dairy products, corn silage
      Latilactobacillus
      Homofermentative.
      Lat.sakei
      Species are the type species for this genus.
      curvatus; dairy products such as milk and cheese, corn or grass silage, cow dung graminis; grass silage
      Lentilactobacillus
      Heterofermentative.
      Len.kefiri; kefir grains parakefiri; kefir grains buchneri
      Species are the type species for this genus.
      ; milk, cheese parabuchneri; dairy products, silage curieae; cheese curd powder diolivorans; silage, fermented dairy products hilgardii; silage parafarraginis; silage, kefir grains
      Levilactobacillus
      Heterofermentative.
      Lev.brevis
      Species are the type species for this genus.
      ; milk, cheese, silage, cow manure parabrevis; cheese angrenensis; fermented dairy beverage hammesii; ryegrass silage
      Ligilactobacillus
      Homofermentative.
      Lig.salivarius
      Species are the type species for this genus.
      ; dairy products acidipiscis; dairy products agilis; cheese
      Limosilactobacillus
      Heterofermentative.
      Lim.fermentum
      Species are the type species for this genus.
      ; dairy products, manure pontis; dairy products, silage gastricus; human milk oris; human milk reuteri; of intestinal origin,
      Loigolactobacillus
      Homofermentative.
      Lo.bifermentans; cheese, fermented milk products coryniformis
      Species are the type species for this genus.
      coryniformis ssp. coryniformis; silage, dairy barn air and sewage. cow dung, cheese coryniformis ssp. torquens; cheese, silage rennini; rennet iwatensis; orchard grass silage
      Paucilactobacillus
      Heterofermentative.
      Pa.hokkaidonensis; grass silage vaccinostercus
      Species are the type species for this genus.
      ; cow dung wasatchensis; cheese, silage suebicus; silage
      Companilactobacillus
      Heterofermentative.
      Co.alimentarius
      Species are the type species for this genus.
      crustorum; fermented dairy product farciminis; dairy products, corn silage zhongbaensis; fermented dairy product
      Amylolactobacillus
      Heterofermentative.
      Am.amylophilus
      Species are the type species for this genus.
      amylotrophicus; corn silage
      Lapidilactobacillus
      Heterofermentative.
      Lap.concavus
      Species are the type species for this genus.
      dextrinicus; silage
      1 Homofermentative.
      2 Species are the type species for this genus.
      3 Heterofermentative.

      LACTOBACILLI AND DAIRY FOODS

      Lactic acid bacteria can be divided into 2 groups relative to fermented dairy foods; starter lactic acid bacteria intentionally added to the milk, and nonstarter lactic acid bacteria (NSLAB) that are part of the milk and production facility microbiota which contaminate the milk or product during production. Fermented dairy products can be divided into 2 major groups, liquid or semisolid products where no liquid has been removed, and products where whey has been removed during manufacture. Liquid and semisolid products include fermented milks and yogurts, whereas cheese manufacture includes a whey-removal step where some water, whey proteins, minerals, and lactose are removed.
      In the manufacture of cheese, starter cultures can be added as mixtures of defined or undefined strains purchased from a culture supplier and added directly to milk, or as a bulk starter culture prepared in the factory with the seed culture purchased from a supplier. In some smaller scale artisan operations, the starter culture is propagated in-house by fermentation of whey from the previous day's production run. In such cases, the fermentation is uncontrolled and strain variations likely occur over time (
      • Beresford T.P.
      • Fitzsimons N.A.
      • Brennan N.L.
      • Cogan T.M.
      Recent advances in cheese microbiology.
      ). The mesophilic Lactococcus lactis is the prime acid-producing starter culture for many cheeses. For cheeses that have a higher cooking temperature, thermophilic starter cultures composed of lactobacilli and Streptococcus thermophilus are employed and are usually the acid-producing bacteria dominant in self-propagated starter cultures.
      The Lactobacillus portion of a starter culture (Table 3) helps control the pH of the fermented product, influences growth of other microorganisms, and causes proteolysis and lipolysis, which influences product texture and formation of specific flavor compounds (
      • Lobo di Palma V.
      • Hammond E.G.
      • Glatz B.A.
      Effect of lactobacilli on the properties of Swiss cheese.
      ). In addition, lactobacilli help provide biopreservation through production of alcohols, organic acids, carbon dioxide, diacetyl, hydrogen peroxide, and other substances capable of inhibiting growth of unwanted microorganisms (
      • Helander I.M.
      • von Wright A.
      • Mattila-Sandholm T.-M.
      Potential of lactic acid bacteria and novel antimicrobials against Gram-negative bacteria.
      ;
      • Ortiz-Rivera Y.
      • Sánchez-Vega R.
      • Gutiérrez-Méndez N.
      • León-Félix J.
      • Acosta-Muñiz C.
      • Sepulveda D.R.
      Production of reuterin in a fermented milk product by Lactobacillus reuteri: Inhibition of pathogens, spoilage microorganisms, and lactic acid bacteria.
      ).
      Table 3Use of Lactobacillus as defined strain acid-producing starter cultures
      ProductOrganismUsageReference
      YogurtLb. delbrueckii ssp. bulgaricus
      Used in conjunction with Streptococcus thermophilus.
      Often legally required in some countries
      • Aryana K.J.
      • Olson D.W.
      A 100-year review: Yogurt and other cultured dairy products.
      Swiss and Dutch CheesesLb. delbrueckii ssp. bulgaricus
      Used in conjunction with Streptococcus thermophilus.
      Lb. delbrueckii ssp. lactis
      Used in conjunction with Streptococcus thermophilus.
      Allows measurement of d- and l-lactate levels to monitor relative bacterial numbers.
      Lb. helveticus
      Used in conjunction with Streptococcus thermophilus.
      Traditional usage was Lb. delbrueckii ssp. bulgaricus but is now more frequently Lb. helveticus
      • Hunter J.E.
      • Frazier W.C.
      Gas production by associated Swiss cheese bacteria.
      • Biede S.L.
      • Reinbold G.W.
      • Hammond E.G.
      Influence of Lactobacillus bulgaricus on commercial Swiss cheese.
      • Reddy K.P.
      • Richardson G.H.
      Lactic bulk culture system utilizing whey-based bacteriophage inhibitory medium and pH control. IV. Applicability to Italian and Swiss cheese cultures.
      • White S.R.
      • Broadbent J.R.
      • Oberg C.J.
      • McMahon D.J.
      Effect of Lactobacillus helveticus and Propionibacterium freudenrichii ssp. shermanii combinations on propensity for split defect in Swiss cheese.
      • Ji T.
      • Alvarez V.B.
      • Harper W.J.
      Influence of starter culture ratios and warm room treatment on free fatty acid and amino acid in Swiss cheese.
      Mozzarella CheeseLb. delbrueckii ssp. bulgaricus
      Either used with S. thermophilus or not used and cheese made using S. thermophilus only.
      Lb. helveticus
      Either used with S. thermophilus or not used and cheese made using S. thermophilus only.
      Lb. helveticus is often used as it has it is able to better ferment galactose
      • Biede S.L.
      • Reinbold G.W.
      • Hammond E.G.
      Influence of Lactobacillus bulgaricus on commercial Swiss cheese.
      • Johnson M.E.
      • Olson N.F.
      Nonenzymatic browning of mozzarella cheese.
      1 Used in conjunction with Streptococcus thermophilus.
      2 Allows measurement of d- and l-lactate levels to monitor relative bacterial numbers.
      3 Either used with S. thermophilus or not used and cheese made using S. thermophilus only.
      Nonstarter lactobacilli exert a wide range of effects on fermented dairy products. Some NSLAB are viewed as a positive or desired addition to the cheese microbiota, whereas others are associated with defects such as slits and cracks, off-flavors, and crystal formation in Cheddar cheese (
      • Crow V.L.
      • Coolbear T.
      • Gopal P.K.
      • Martley F.G.
      • McKay L.L.
      • Riepe H.
      The role of autolysis of lactic acid bacteria in the ripening of cheese.
      ;
      • Broadbent J.R.
      • Houck K.
      • Johnson M.E.
      • Oberg C.J.
      Influence of adjunct use and cheese microenvironment on nonstarter bacteria in reduced-fat Cheddar-type cheese.
      ). The NSLAB enter the cheese because they either survive pasteurization or are introduced postpasteurization from the dairy plant environment and often become the predominate bacteria in Cheddar cheese at the time of sale (
      • Oberg C.J.
      • Moyes L.V.
      • Domek M.J.
      • Brothersen C.F.
      • McMahon D.J.
      Survival of probiotic adjunct cultures in cheese and challenges in their enumeration using selective media.
      ).

      LACTOBACILLI USED AS STARTER CULTURES

      Species Associated with Yogurt and Fermented Milks

      Yogurt starter cultures require a symbiotic blend of Lactobacillus delbrueckii ssp. bulgaricus and S. thermophilus to achieve the desired organoleptic properties such as texture, acidity, and flavor (
      • Oyeniran A.
      • Ibrahim S.A.
      • Gyawali R.
      • Tahergorabi R.
      • Zimmerman T.
      • Krastanov A.
      A modified reinforced clostridial medium for the isolation and enumeration of Lactobacillus delbrueckii ssp. bulgaricus in a mixed culture.
      ). Streptococcus thermophilus has urease genes and its production of NH3 has a stimulatory effect on Lb. delbrueckii ssp. bulgaricus, therefore, urease activity is an essential factor for effective yogurt acidification (
      • Yamauchi R.
      • Maguin E.
      • Horiuchi H.
      • Hosokawa M.
      • Sasaki Y.
      The critical role of urease in yogurt fermentation with various combinations of Streptococcus thermophilus and Lactobacillus delbrueckii ssp. bulgaricus..
      ). Many countries have legal requirements for the minimum number (such as 107/g) of yogurt starter bacteria or viable lactobacilli, and for the ratio of Lb. delbrueckii ssp. bulgaricus to S. thermophilus (
      • Oyeniran A.
      • Ibrahim S.A.
      • Gyawali R.
      • Tahergorabi R.
      • Zimmerman T.
      • Krastanov A.
      A modified reinforced clostridial medium for the isolation and enumeration of Lactobacillus delbrueckii ssp. bulgaricus in a mixed culture.
      ).
      Fermented milks have a long history of production in many parts of the world and include kefir and koumiss, cultured buttermilk, mesophilic cultured milks such as ilmjolk, tatmjolk and langofil, thermophilic cultured milks such as Bulgarian buttermilk, zabadi, dahi, and biotherapeutic type products such as sweet acidophilus milk.

      Lactobacillus delbrueckii ssp. bulgaricus

      Lactobacillus delbrueckii is the type species for the Lactobacillus genus. Lactobacillus delbrueckii ssp. bulgaricus ferments glucose to lactic acid and also metabolizes fructose, mannose, and lactose, but not galactose or sucrose. This subspecies was previously referred to as Lactobacillus bulgaricus and was originally isolated from yogurt (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Lactobacillus delbrueckii is the type species for the Lactobacillus genus. Lactobacillus delbrueckii ssp. bulgaricus ferments glucose to lactic acid and also metabolizes fructose, mannose and lactose, but not galactose or sucrose. This subspecies was previously referred to as Lactobacillus bulgaricus and was originally isolated from yogurt.
      For use as a starter culture in yogurt, both the flavor production and acid-producing characteristics of Lb. delbrueckii ssp. bulgaricus are important. There are differences between strains of this species in terms of fermentation time, acidification rate, and acetaldehyde production. Natural selection pressure and the environmental stress conditions of yogurt can result in selection of strains yielding different acetaldehyde concentrations that can be an issue in yogurt manufacture (
      • Liu W.
      • Yu J.
      • Sun Z.
      • Song Y.
      • Wang X.
      • Wang H.
      • Wuren T.
      • Zha M.
      • Menghe B.
      • Heping Z.
      Relationships between functional genes in Lactobacillus delbrueckii ssp. bulgaricus isolates and phenotypic characteristics associated with fermentation time and flavor production in yogurt elucidated using multilocus sequence typing.
      ). Some Lb. delbrueckii ssp. bulgaricus strains produce extracellular polysaccharides, which act as food stabilizers to prevent syneresis and graininess, and provide the product with natural thickness (
      • Cerning J.
      Exocellular polysaccharides produced by lactic acid bacteria.
      ;
      • Rizzello C.G.
      • De Angelis M.
      Lactobacillus delbrueckii group.
      ). Lactobacillus delbrueckii ssp. bulgaricus is also regarded as having probiotic properties (
      • Oyeniran A.
      • Ibrahim S.A.
      • Gyawali R.
      • Tahergorabi R.
      • Zimmerman T.
      • Krastanov A.
      A modified reinforced clostridial medium for the isolation and enumeration of Lactobacillus delbrueckii ssp. bulgaricus in a mixed culture.
      ).
      Strains of Lb. delbrueckii ssp. bulgaricus have also been a traditional starter culture for Swiss (
      • Biede S.L.
      • Reinbold G.W.
      • Hammond E.G.
      Influence of Lactobacillus bulgaricus on commercial Swiss cheese.
      ) and Italian cheeses although it is now often replaced by Lactobacillus helveticus (
      • White S.R.
      • Broadbent J.R.
      • Oberg C.J.
      • McMahon D.J.
      Effect of Lactobacillus helveticus and Propionibacterium freudenrichii ssp. shermanii combinations on propensity for split defect in Swiss cheese.
      ), which has the ability to ferment galactose (
      • Johnson M.E.
      • Olson N.F.
      Nonenzymatic browning of mozzarella cheese.
      ). In the manufacture of Swiss cheese, the ratio of Lb. delbrueckii ssp. bulgaricus compared with S. thermophilus in the starter culture influences the chemistry and flavor of Swiss cheese through changes in its microbiota. Using Lb. delbrueckii ssp. bulgaricus increases flavor intensity, yet there is an optimum level above which numbers of propionibacteria decrease, which retards flavor development (
      • Biede S.L.
      • Reinbold G.W.
      • Hammond E.G.
      Influence of Lactobacillus bulgaricus on commercial Swiss cheese.
      ).

      Lactobacillus acidophilus

      Lactobacillus acidophilus grows optimally at 35 to 40°C, but it is able to grow at temperatures as high as 45°C and is an homofermentative lactic acid bacterium producing lactic acid and carbon dioxide through the Embden-Meyerhof-Parnas pathway (
      • Ozogul F.
      • Yazgan H.
      • Ozogul Y.
      Lactic acid bacteria: Lactobacillus acidophilus.
      ). The usual method for enumerating Lb. acidophilus in yogurt and other dairy products is with de Man, Rogosa, and Sharpe (MRS) agar (pH 5.4), incubated anaerobically at 45°C, which inhibits S. thermophilus; however, other lactobacilli that may be present in the product can grow in this medium (
      • Ozogul F.
      • Yazgan H.
      • Ozogul Y.
      Lactic acid bacteria: Lactobacillus acidophilus.
      ).
      In the United States, perhaps the first dairy food commercially manufactured and marketed for health promoting benefits was sweet acidophilus milk made using Lb. acidophilus. The higher pH of nonfermented products such as sweet acidophilus milk provides for longer survival. In mixed cultures, growth of Lb. acidophilus during fermentation is much slower than other lactobacilli and S. thermophilus. Instability of Lb. acidophilus in yogurt can be caused by hydrogen peroxide production by other lactobacilli (
      • Ozogul F.
      • Yazgan H.
      • Ozogul Y.
      Lactic acid bacteria: Lactobacillus acidophilus.
      ). When Lb. acidophilus is added in cheesemaking as an adjunct culture for its probiotic potential, its persistence during cheese aging can change the flavor profile of the cheese and, hence, its consumer acceptability (
      • Gomes A.A.
      • Braga S.P.
      • Cruz A.G.
      • Cadena R.S.
      • Lollo P.C.B.
      • Carvalho C.
      • Amaya-Farfán J.
      • Faria J.A.F.
      • Bolini H.M.A.
      Effect of the inoculation level of Lactobacillus acidophilus in probiotic cheese on the physicochemical features and sensory performance compared with commercial cheeses.
      ). Measurement of Lb. acidophilus persistence in cheese during its shelf life is difficult as many NSLAB can grow under the same conditions used to enumerate Lb. acidophilus (
      • Oberg C.J.
      • Moyes L.V.
      • Domek M.J.
      • Brothersen C.F.
      • McMahon D.J.
      Survival of probiotic adjunct cultures in cheese and challenges in their enumeration using selective media.
      ).
      Lactobacillus acidophilus is also used in the manufacture of yogurt, yogurt drinks, iru-miru, kefir, fermented desserts, and koumiss (
      • Ozogul F.
      • Yazgan H.
      • Ozogul Y.
      Lactic acid bacteria: Lactobacillus acidophilus.
      ). The organism is considered a probiotic bacterium for which a minimal level of viability for a specified strain in the product needs to be maintained if the product carries any type of health claim. Many Lb. acidophilus strains inhibit gram-positive and gram-negative bacteria, a result of production of a combination of hydrogen peroxide, organic acid, and bacteriocins such as lactocin B, lactacin F, acidocin A, and acidocin B (
      • Ozogul F.
      • Yazgan H.
      • Ozogul Y.
      Lactic acid bacteria: Lactobacillus acidophilus.
      ).

      Lactobacillus kefiranofaciens

      This homofermentative species produces lactic acid from a variety of sugars including glucose, fructose, galactose, sucrose, maltose, lactose and raffinose, but not from arabinose, ribose, cellobiose, or trehalose (
      • Vancanneyt M.
      • Mengaud J.
      • Cleenwerck I.
      • Vanhonacker K.
      • Hoste B.
      Reclassification of Lactobacillus kefirgranum Takizawa et al. 1994 as Lactobacillus kefiranofaciens subsp. kefirgranum subsp. nov. and emended description of L. kefiranofaciens Fujisawa et al. 1988.
      ). Two subspecies are recognized: Lactobacillus kefiranofaciens ssp. kefiranofaciens and Lactobacillus kefiranofaciens ssp. kefirgranum.
      Fermentation of milk using a combination of bacteria and yeasts (such as Kluyveromyces marxianus, Saccharomyces cerevisiae, and Kazachatania unispora) developed in central Asia (north of the Caucasus mountains) at least 2,000 years ago. Kefir and similar fermented milks have undergone continuous harvesting of the starter culture (Table 4) and propagation in homes since that time. Kefir grains resemble miniature cauliflower florets and consist of a symbiotic mixture of yeasts, lactobacilli, lactococci, and Leuconostoc species (Aryana and Olsen, 2017). The dominant and most consistent lactobacilli in kefir grains is Lactobacillus kefiranofaciens (
      • Wang X.
      • Xiao J.
      • Jia Y.
      • Pan Y.
      • Wang Y.
      Lactobacillus kefiranofaciens, the sole dominant and stable bacterial species, exhibits distinct morphotypes upon colonization in Tibetan kefir grains.
      ).
      Table 4Lactobacilli
      Genus abbreviations as described in Table 2.
      that have been shown to be present in kefir grains
      Predominant lactobacilliOther lactobacilliReferences
      Lb. kefiranofaciens ssp. kefiranofaciens Lb kefiranofaciens ssp. kefirgranumLb. delbrueckii Lb. acidophilus Lev. brevis Lb. helveticus Lcb. casei Lcb. paracasei Lim. fermentum Lpb. plantarum Lb. gasseri Len. sunkii Len. kefiri Len. parakefiri
      • Wang X.
      • Xiao J.
      • Jia Y.
      • Pan Y.
      • Wang Y.
      Lactobacillus kefiranofaciens, the sole dominant and stable bacterial species, exhibits distinct morphotypes upon colonization in Tibetan kefir grains.
      • Magalhães K.T.
      • Pereira M.A.
      • Nicolau A.
      • Dragone G.
      • Domingues L.
      • Teixeira J.A.
      • de Almeida Silva J.B.
      • Schwan R.F.
      Production of fermented cheese whey-based beverage using kefir grains as starter culture: Evaluation of morphological and microbial variations.
      • Vardjan T.
      • Mohar Lorbeg P.
      • Rogelj I.
      • Canzek Majhenic A.
      Characterization and stability of lactobacilli and yeast microbiota in kefir grains.
      • Huang Y.
      • Wu F.
      • Wang X.
      • Sui Y.
      • Yang L.
      • Wang J.
      Characterization of Lactobacillus plantarum Lp27 isolated from Tibetan kefir grains: A potential probiotic bacterium with cholesterol-lowering effects.
      • Kandler O.
      • Schillinger U.
      • Weiss N.
      Lactobacillus bifermentans sp. nov., nom. rev., an organism forming CO(2) and H(2) from lactic acid.
      1 Genus abbreviations as described in Table 2.
      Kefir grains are held together by a complex mixture of protein and a polysaccharide (kefirin) that is a component of the capsular material of Lentilactobacillus parakefiri and Lb. kefiranofaciens, which are the major exopolysaccharide (EPS)-producing bacteria present in kefir grains (
      • Kök-Taş T.
      • Ekinci F.Y.
      • Guzel-Seydim Z.B.
      Identification of microbial flora in kefir grains produced in Turkey using PCR.
      ). Certain strains of Lb. kefiranofaciens have demonstrated probiotic properties (
      • Vinderola G.
      • Perdigón G.
      • Duarte J.
      • Farnworth E.
      • Matar C.
      Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity.
      ;
      • Furuno T.
      • Nakanishi M.
      Kefiran suppresses antigen-induced mast cell activation.
      ). Propagating the kefir grains in milk is important for maintaining the dominant lactobacilli otherwise other species begin to dominate (
      • Zanirati D.F.
      • Abatemarco Jr., M.
      • Sandes S.H.C.
      • Nicoli J.B.
      • Nunes A.C.
      • Neumann E.
      Selection of lactic acid bacteria from Brazilian kefir grains for potential use as starter or probiotic cultures.
      ). In traditional kefir, although lactic acid is the main fermentative metabolite, small amounts of alcohol and carbon dioxide are also produced by the yeast present in the kefir grain giving a pronounced effervescence typical of kefir.

      Lentilactobacillus kefiri

      The genus Lentilactobacillus was so called because of the slow growth of species in the genus with lactate or propanediol as carbon source (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Formerly known as Lactobacillus kefir or Lactobacillus kefiri, this organism is mainly found as part of the microbiota of kefir grains and kefir drinks (
      • Kandler O.
      • Schillinger U.
      • Weiss N.
      Lactobacillus bifermentans sp. nov., nom. rev., an organism forming CO(2) and H(2) from lactic acid.
      ) but has also been isolated from Camembert cheese, in ricotta forte (
      • Baruzzi F.
      • Morea M.
      • Matarante A.
      • Cocconcelli P.S.
      Changes in the Lactobacillus community during Ricotta forte cheese natural fermentation.
      ) and in raw camel milk (
      • Akhmetsadykova S.H.
      • Baubekova A.
      • Konuspayeva G.
      • Akhmetsadykov N.
      • Faye B.
      • Loiseau G.
      Lactic acid bacteria biodiversity in raw and fermented camel milk.
      ).

      Lentilactobacillus parakefiri

      Lentilactobacillus parakefiri is very closely related to, but distinct from, Len. kefiri. A heterofermentative organism, it produces l-lactic acid, and CO2 from glucose, but not from gluconate (
      • Takizawa S.
      • Kojima S.
      • Tamura S.
      • Fujinaga S.
      • Benno Y.
      • Nakase T.
      Lactobacillus kefirgranum sp. nov. and Lactobacillus parakefir sp. nov., two new species from kefir grains.
      ). It was originally isolated from kefir grains but has been recently identified as a predominant LAB in butter (
      • Syromyatnikov M.Y.
      • Kokina A.V.
      • Solodskikh S.A.
      • Panevina A.V.
      • Popov E.S.
      • Popov V.N.
      High-throughput 16S rRNA gene sequencing of butter microbiota reveals a variety of opportunistic pathogens.
      ).

      Lentilactobacillus sunkii

      Lentilactobacillus sunkii has been isolated from kefir (
      • Han X.
      • Zhang L.J.
      • Wu H.Y.
      • Wu Y.F.
      • Zhao S.N.
      Investigation of microorganisms involved in kefir biofilm formation.
      ), but was originally isolated from sunki, a type of Japanese pickle (
      • Watanabe K.
      • Fujimoto J.
      • Tomii Y.
      • Sasamoto M.
      • Makino H.
      • Kudo Y.
      • Okada S.
      Lactobacillus kisonensis sp. nov., Lactobacillus otakiensis sp. nov., Lactobacillus rapi sp. nov. and Lactobacillus sunkii sp. nov., heterofermentative species isolated from sunki, a traditional Japanese pickle.
      ). It is a heterofermentative organism producing lactic acid and gas from glucose metabolism.

      Species Associated with Cheese

      Lactobacillus helveticus

      Lactobacillus helveticus is homofermentative. All strains of Lb. helveticus ferment glucose, galactose, and lactose, whereas some strains also ferment fructose, maltose, mannose and trehalose. Lactobacillus helveticus does not use pentoses, cellobiose, mannitol, raffinose, sucrose, or gluconate (
      • Nikoloudaki O.
      • Gobbetti M.
      • Di Cango R.
      Lactic acid bacteria: Lactobacillus helveticus.
      ).
      Lactobacillus helveticus can be used in the manufacture of Swiss and Dutch style cheeses instead of Lb. delbrueckii ssp. bulgaricus because of its ability to ferment galactose. Another distinction is that Lb. helveticus produces both d- and l-lactate, whereas Lb. delbrueckii ssp. bulgaricus only produces the d-lactate isomer, which may be of advantage in Swiss cheese manufacture as the l-lactate isomer is preferred by propionibacteria (
      • Nikoloudaki O.
      • Gobbetti M.
      • Di Cango R.
      Lactic acid bacteria: Lactobacillus helveticus.
      ). Later, when placed in a warm room (∼20 to 22°C) it is primarily l-lactate that is used by Propionibacterium freudenreichii, as this results in a high intracellular pyruvate concentration that inhibits d-lactate dehydrogenase activity (
      • White S.R.
      • Broadbent J.R.
      • Oberg C.J.
      • McMahon D.J.
      Effect of Lactobacillus helveticus and Propionibacterium freudenrichii ssp. shermanii combinations on propensity for split defect in Swiss cheese.
      ).
      The most commonly used lactobacilli now in the starter culture for Swiss cheese is Lb. helveticus (
      • White S.R.
      • Broadbent J.R.
      • Oberg C.J.
      • McMahon D.J.
      Effect of Lactobacillus helveticus and Propionibacterium freudenrichii ssp. shermanii combinations on propensity for split defect in Swiss cheese.
      ;
      • Ji T.
      • Alvarez V.B.
      • Harper W.J.
      Influence of starter culture ratios and warm room treatment on free fatty acid and amino acid in Swiss cheese.
      ), replacing Lb. delbrueckii ssp. bulgaricus (
      • Reddy K.P.
      • Richardson G.H.
      Lactic bulk culture system utilizing whey-based bacteriophage inhibitory medium and pH control. IV. Applicability to Italian and Swiss cheese cultures.
      ). In Swiss cheese, Lb. helveticus is the secondary acid producer to S. thermophilus, provides proteolysis in the later stages of ripening, and contributes to flavor development. During manufacture up until brining d- or l-lactic acid are essentially the only end products of lactose fermentation. After brining is when the selection of Lb. helveticus or Lb. delbrueckii ssp. bulgaricus has greater effect. For example, differences in their cell wall proteases result in Swiss cheese made using Lb. helveticus having greater stretchability than when made using Lb. delbrueckii ssp. lactis (
      • Richoux R.
      • Aubert L.
      • Roset G.
      • Kerjean J.R.
      Impact of the proteolysis due to lactobacilli on the stretchability of Swisstype cheese.
      ;
      • Sadat-Mekmene L.
      • Richoux R.
      • Aubert-Frogerais L.
      • Madec M.-N.
      • Corre C.
      • Piot M.
      • Jardin J.
      • le Feunteun S.
      • Lortal S.
      • Gagnaire V.
      Lactobacillus helveticus as a tool to change proteolysis and functionality in Swiss-type cheeses.
      ).
      In the whey culture (Table 5) used for manufacture of Italian cultures hard cheeses such as Parmigiano Reggiano, the dominant species is Lb. helveticus along with Lb. delbrueckii ssp. bulgaricus, Lb. delbrueckii ssp. lactis, Lacticaseibacillus casei, Limosilactobacillus fermentum, and S. thermophilus (
      • Reinheimer J.A.
      • Suárez V.B.
      • Bailo N.B.
      • Zalazar C.A.
      Microbiological and technological characteristics of natural whey cultures for Argentinean hard cheese production.
      ;
      • Gatti M.
      • Lazzi C.
      • Rossetti L.
      • Mucchetti G.
      • Neviani E.
      Biodiversity in Lactobacillus helveticus strains present in natural whey starter used for Parmigiano Reggiano cheese.
      ;
      • Bottari B.
      • Santarelli M.
      • Neviani E.
      • Gatti M.
      Natural whey starter for Parmigiano Reggiano: Culture-independent approach.
      ). In Argentina, the whey starter used for Reggianito Argentino cheese consisted of 66% Lb. helveticus strains and 33% of Lb. delbrueckii ssp. lactis (
      • Reinheimer J.
      • Quiberoni A.
      • Tailliez P.
      • Binetti A.
      • Suárez V.
      The lactic acid microflora of natural whey starters used in Argentina on hard cheese production.
      ). Various biotypes occur in Lb. helveticus strains in whey starters with differences in fructose, maltose, and trehalose fermentation, acidifying activity, proteolytic and peptidase activity, and antibiotic and lysozyme resistance (
      • Fortina M.G.
      • Nicastro G.
      • Carminati D.
      • Neviani E.
      • Manachini P.L.
      Lactobacillus helveticus heterogeneity in natural cheese starters: the diversity in phenotypic characteristics.
      ). Often a characteristic of such whey starters is a low salt tolerance of the strains (
      • Reinheimer J.
      • Quiberoni A.
      • Tailliez P.
      • Binetti A.
      • Suárez V.
      The lactic acid microflora of natural whey starters used in Argentina on hard cheese production.
      ). Replacement of the whey starter with defined strains of Lb. helveticus can produce cheese with comparable flavor, and
      • Hynes E.R.
      • Bergamini C.V.
      • Suárez V.B.
      • Zalazar C.A.
      Proteolysis on Reggianito Argentino cheeses manufactured with natural whey cultures and selected strains of Lactobacillus helveticus..
      found that such cheeses did not group by Lb. helveticus strain or type of starter when analyzed for flavor. Lactobacillus helveticus is used as a flavor adjunct (Table 6) in Cheddar manufacture adds sweet-nutty aspects to the flavor profile and prevents bitterness (
      • Madkor S.A.
      • Tong P.S.
      • El Soda M.
      Ripening of cheddar cheese with added attenuated adjunct cultures of lactobacilli.
      ).
      Table 5Lactobacilli
      Genus abbreviations as described in Table 2.
      identified as part of in-factory propagated whey starter cultures
      Cheese type (location)Predominant bacteriaOther bacteriaReference
      Gruyère Emmental Grana (France, Switzerland, Italy)Streptococcus thermophilusLactococcus sp. Leuconostoc sp. Lb. helveticus Lb. delbrueckii Lb. acidophilus Lim. fermentum
      • Beresford T.P.
      • Fitzsimons N.A.
      • Brennan N.L.
      • Cogan T.M.
      Recent advances in cheese microbiology.
      Parmigiano Reggiano (Italy)Lb. helveticusLb. delbrueckii ssp. bulgaricus Lb. delbrueckii ssp. lactis Lcb. casei Lm. fermentum S. thermophilus
      • Beresford T.P.
      • Fitzsimons N.A.
      • Brennan N.L.
      • Cogan T.M.
      Recent advances in cheese microbiology.
      • Nikoloudaki O.
      • Gobbetti M.
      • Di Cango R.
      Lactic acid bacteria: Lactobacillus helveticus.
      • Reinheimer J.A.
      • Suárez V.B.
      • Bailo N.B.
      • Zalazar C.A.
      Microbiological and technological characteristics of natural whey cultures for Argentinean hard cheese production.
      • Gatti M.
      • Lazzi C.
      • Rossetti L.
      • Mucchetti G.
      • Neviani E.
      Biodiversity in Lactobacillus helveticus strains present in natural whey starter used for Parmigiano Reggiano cheese.
      • Bottari B.
      • Santarelli M.
      • Neviani E.
      • Gatti M.
      Natural whey starter for Parmigiano Reggiano: Culture-independent approach.
      Reggianito Argentino (Argentina)Lb. helveticus Lb. delbrueckii ssp. lactis
      • Reinheimer J.
      • Quiberoni A.
      • Tailliez P.
      • Binetti A.
      • Suárez V.
      The lactic acid microflora of natural whey starters used in Argentina on hard cheese production.
      Caciocavallo Silano and Grana Padano cheeses (Italy)Lim. fermentum
      • Rossetti L.
      • Fornasari M.E.
      • Gatti M.
      • Lazzi C.
      • Neviani E.
      • Giraffa G.
      Grana Padano cheese whey starters: Microbial composition and strain distribution.
      1 Genus abbreviations as described in Table 2.
      Table 6Historical view of nonstarter lactobacilli
      Genus abbreviations as described in Table 2.
      in Cheddar cheese
      Time periodCountryDominant lactobacilliOther lactobacilli presentReference
      1930sNew ZealandLpb. plantarumLcb. paracasei/casei
      Many species classified previously (before ~1990) as Lactobacillus casei were most likely Lactobacillus paracasei (Minervini and Calasso, 2020), and most genomes designated as Lb. casei in the National Center for Biotechnology Information database (https://ncbi.nlm.nih.gov) database should be classified as Lb. paracasei as well (Zheng et al., 2020).
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      1960sLcb. casei/paracaseiLpb. plantarum, Lev. brevis
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      1990sUnited KingdomLcb. casei/paracasei Lpb. plantarumLat. curvatus, Lev. brevis Lb. helveticus, Lim. fermentum, Lo. bifermentans, Len. buchneri, Len. parabuchneri, Len. kefiri Co. farciminis
      • Williams A.G.
      • Banks J.M.
      Proteolytic and other hydrolytic enzyme activities in non-starter lactic acid bacteria (NSLAB) isolated from Cheddar cheese manufactured in the United Kingdom.
      2020USA and IrelandLcb. paracasei Lcb. rhamnosus Lcb. delbrueckii
      Possibly added as an adjunct starter culture.
      Lb. helveticus
      Possibly added as an adjunct starter culture.
      Lat. curvatus Pa. wasatchensis Se. malefermentans
      Lcb. casei, Lcb. paracasei Lcb. rhamnosus Lpb. plantarum Lb. delbrueckii, Lb. helveticus Lb. hokkaidonensis, Lb. crispatus Lat. curvatus Len. buchneri, Len. farraginis Len. kefiri, Len. kisonensis Pa. wasatchensis, Lo. coryniformis, Lo. coryniformis ssp. torquens
      • Overbeck S.L.
      Comparison of microbial diversity of fifteen aged Cheddar cheeses from different regions using next generation sequencing.
      1 Genus abbreviations as described in Table 2.
      2 Many species classified previously (before ~1990) as Lactobacillus casei were most likely Lactobacillus paracasei (Minervini and Calasso, 2020), and most genomes designated as Lb. casei in the National Center for Biotechnology Information database (https://ncbi.nlm.nih.gov) database should be classified as Lb. paracasei as well (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ).
      3 Possibly added as an adjunct starter culture.

      Lactobacillus delbrueckii ssp. lactis

      This subspecies of Lb. delbrueckii has traditionally been one of the lactobacilli used as a starter culture in Swiss-type cheeses along with Lb. delbrueckii ssp. bulgaricus and Lb. helveticus (
      • Hunter J.E.
      • Frazier W.C.
      Gas production by associated Swiss cheese bacteria.
      ). Lactobacillus delbrueckii ssp. lactis is also used as a starter culture in Emmental and Gruyère-type cheeses (
      • Weinrichter B.
      • Sollberger H.
      • Ginzinger W.
      • Jaros D.
      • Rohm H.
      Adjunct starter properties affect characteristic features of Swiss-type cheeses.
      ). Traditional production Ragusano cheese in Italy use wooden vessels that carry a biofilm on their surface that inoculates and acidifies the milk. The dominant species in these biofilms are S. thermophilus and Lb. delbrueckii ssp. lactis (
      • Licitra G.
      • Ogier J.C.
      • Parayre S.
      • Pediliggieri C.
      • Carnemolla T.M.
      • Falentin H.
      • Madec M.N.
      • Carpino S.
      • Lortal S.
      Variability of bacterial biofilms of the “tina” wood vats used in the ragusano cheese-making process.
      ).

      LACTOBACILLI ISOLATED FROM MILK AND DAIRY PRODUCTS

      In products such as cheese, there is a secondary microbiota that develops during product ripening and storage, which can consist of complex mixtures of bacteria, yeasts, and molds, depending on the particular cheese variety (
      • Beresford T.P.
      • Fitzsimons N.A.
      • Brennan N.L.
      • Cogan T.M.
      Recent advances in cheese microbiology.
      ). Before the onset of DNA sequencing technologies to identify NSLAB in cheese, only those bacteria that could be cultured from the cheese were identified (Table 6). Some traditional cheeses made without addition of any starter culture rely upon endogenous lactic acid bacteria in the raw milk to bring about fermentation (
      • Efthymiou C.C.
      • Mattick J.F.
      Development of domestic Feta cheese.
      ;
      • Di Cagno R.
      • Buchin S.
      • de Candia S.
      • De Angelis M.
      • Fox P.F.
      • Gobbetti M.
      Characterization of Italian cheeses ripened under nonconventional conditions.
      ). Such cheeses typically contain both homofermentative and heterofermentative lactic acid bacteria including Lacticaseibacillus paracasei, Lactiplantibacillus plantarum, and Levilactobacillus brevis, generally considered NSLAB (
      • Di Cagno R.
      • Buchin S.
      • de Candia S.
      • De Angelis M.
      • Fox P.F.
      • Gobbetti M.
      Characterization of Italian cheeses ripened under nonconventional conditions.
      ). These NSLAB lactobacilli can be isolated, characterized, then used as adjunct cultures (Table 7) to the starter cultures to provide added benefits to the final product such as enhanced flavor, more rapid flavor development, and even inhibition of undesirable bacteria during storage.
      Table 7Lactobacilli
      Genus abbreviations as described in Table 2.
      Beneficial and detrimental effects of adjunct cultures are strain dependent (Stefanovic et al., 2017a).
      used as adjunct cultures in cheese
      BacteriaPurposeReferences
      Lcb. casei Lcb. paracaseiFlavor, probiotic, control of other bacteriaMinervini and Calasso, 2020
      • Lynch C.M.
      • McSweeney P.L.H.
      • Fox P.F.
      • Cogan T.M.
      • Drinan F.D.
      Manufacture of Cheddar cheese with and without adjunct lactobacilli under controlled microbiological conditions.
      • Kocaoglu-Vurma N.A.
      • Harper W.J.
      • Drake M.A.
      • Courtney P.D.
      Microbiological, chemical, and sensory characteristics of Swiss cheese manufactured with adjunct Lactobacillus strains using a low cooking temperature.
      Lcb. rhamnosusPreventing bitterness, control of other heterofermentative lactobacilli that can cause late blowing, biopreservative
      • Kocaoglu-Vurma N.A.
      • Harper W.J.
      • Drake M.A.
      • Courtney P.D.
      Microbiological, chemical, and sensory characteristics of Swiss cheese manufactured with adjunct Lactobacillus strains using a low cooking temperature.
      • Laleye L.C.
      • Simard R.E.
      • Lee B.H.
      • Holley R.A.
      Control of heterofermentative bacteria during Cheddar cheese maturation by homofermentative Lactobacillus starters.
      Lpb. plantarumFlavor
      • Lynch C.M.
      • McSweeney P.L.H.
      • Fox P.F.
      • Cogan T.M.
      • Drinan F.D.
      Manufacture of Cheddar cheese with and without adjunct lactobacilli under controlled microbiological conditions.
      Lb. helveticusAdd sweet nutty flavor to Cheddar cheese
      • Madkor S.A.
      • Tong P.S.
      • El Soda M.
      Ripening of cheddar cheese with added attenuated adjunct cultures of lactobacilli.
      Co. nodensisIncrease sulfur flavor notes
      • O'Brien E.
      • Mills S.
      • Dobson A.
      • Serrano L.M.
      • Hannon J.
      • Ryan S.P.
      • Kilcawley K.N.
      • Brandsma J.B.
      • Meijer W.C.
      • Hill C.
      • Ross R.P.
      Contribution of the novel sulfur-producing adjunct Lactobacillus nodensis to flavor development in Gouda cheese.
      1 Genus abbreviations as described in Table 2.
      2 Beneficial and detrimental effects of adjunct cultures are strain dependent (
      • Stefanovic E.
      • Thierry A.
      • Maillard M.
      • Bertuzzi A.
      • Rea M.C.
      • Fitzgerald G.
      • McAuliffe O.
      • Kilcawley K.N.
      Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems.
      ).
      Adjunct cultures can also be attenuated (such as by freezing, drying, or heat shocking) to provide a mixture of viable and nonviable bacterial cells. Use of adjunct cultures (Table 7) must be considered on an individual basis because of wide strain diversity, such as the ability of strains of Lacticaseibacillus casei and Lacticaseibacillus paracasei to metabolize amino acids in cheese into flavor compounds (
      • Stefanovic E.
      • Thierry A.
      • Maillard M.
      • Bertuzzi A.
      • Rea M.C.
      • Fitzgerald G.
      • McAuliffe O.
      • Kilcawley K.N.
      Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems.
      ). Among lactobacilli isolated from cheese, some can grow and ferment milk relatively quickly (reaching pH 4.5 within 8 h at 34°C), whereas others are slow strains that required supplementation with glucose or casein hydrolysate, and even with supplementation, some strains still do not grow in milk (
      • Briggiler-Marcó M.
      • Capra M.L.
      • Quiberoni A.
      • Vinderola G.
      • Reinheimer J.A.
      • Hynes E.
      Nonstarter Lactobacillus strains as adjunct cultures for cheese making: in vitro characterization and performance in two model cheeses.
      ). Selecting strains that have little effect on acidification would be preferred for use as a flavor adjunct culture so as to not interfere with the time schedule during cheese manufacture.
      The genus Lacticaseibacillus is homofermentative; some but not all species metabolize pentoses via the phosphoketolase pathway (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). In addition to their use as adjuncts, several Lacticaseibacillus species are used as starter cultures in dairy fermentations and as probiotics.

      Adjunct Species Associated with Cheese

      Lacticaseibacillus casei

      The genus name of Lacticaseobacillus refers to the casei-group lactobacilli with Lcb. casei being differentiated from most lactobacilli by many strains exhibiting catalase activity (
      • Wuyts S.
      • Wittouck S.
      • De Boeck I.
      • Allonsius C.N.
      • Pasolli E.
      • Segata N.
      • Lebeer S.
      Large-scale phylogenomics of the Lactobacillus casei group highlights taxonomic inconsistencies and reveals novel clade-associated features.
      ). Information on the lifestyle of Lcb. casei is confounded by the unclear taxonomy during the past decades. In dairy literature before 1989, many strains then classified as Lactobacillus casei were probably Lcb. paracasei (
      • Minervini F.
      • Calasso M.
      Lactobacillus casei group.
      ) and most genomes designated as Lcb. casei in the National Center for Biotechnology Information database (https://ncbi.nlm.nih.gov) should instead be classified as Lcb. paracasei (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ).
      Although first isolated from cheese, Lcb. casei is widely distributed in diverse habitats including decaying plant material, silage, and the human reproductive and gastrointestinal tracts. Because of its aciduric nature, it is also found in many fermented foods of both plant (e.g., fermented vegetables, sourdough, wine) and animal (e.g., dairy products, cured meat, fermented sausages) origin (Minervini and Calasso, 2020). Lacticaseibacillus casei has been most often identified as the main adventitious bacteria (NSLAB) present and growing in ripening cheese, although this is a distinction it now shares with Latilactobacillus curvatus (
      • Broadbent J.R.
      • Houck K.
      • Johnson M.E.
      • Oberg C.J.
      Influence of adjunct use and cheese microenvironment on nonstarter bacteria in reduced-fat Cheddar-type cheese.
      ).
      The use of selected strains of Lcb. casei as adjuncts for cheese ripening or as probiotic cultures in various foods has been continually increasing. Depending on the strain, Lcb. casei can contribute to positive flavor attributes of cheese, to defects, or have no effect on cheese ripening, which is also influenced by cell density and the cheesemaking technology (Minervini and Calasso, 2020).
      Using a homofermentative lactobacilli as an adjunct culture (such as Lcb. casei, Lcb. paracasei, and Lactiplantibacillus plantarum) can inhibit growth of heterofermentative lactobacilli such as Levilactobacillus brevis and Limosilactobacillus fermentum (
      • Laleye L.C.
      • Simard R.E.
      • Lee B.H.
      • Holley R.A.
      Control of heterofermentative bacteria during Cheddar cheese maturation by homofermentative Lactobacillus starters.
      ). Adding the adjunct culture, Lcb. casei, when making cheese can also change the initial NSLAB biota resulting in a reduction in nonstarter species and strain diversity (
      • Broadbent J.R.
      • Houck K.
      • Johnson M.E.
      • Oberg C.J.
      Influence of adjunct use and cheese microenvironment on nonstarter bacteria in reduced-fat Cheddar-type cheese.
      ).

      Lacticaseibacillus paracasei

      Lacticaseibacillus paracasei includes strains previously referred to as Lactobacillus casei ssp. alactosus, Lactobacillus casei ssp. pseudoplantarum, and Lactobacillus casei ssp. tolerans (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Growth of Lcb. paracasei generally occurs over the range of 10 to 40°C, but some strains can grow at 5°C and some up to 45°C. Lacticaseibacillus paracasei cannot ferment rhamnose which distinguishes it from Lacticaseibacillus rhamnosus (Minervini and Calasso, 2020).
      Although not as proteolytic as Lb. helveticus, most strains of Lcb. paracasei have at least one cell envelope-associated serine-type proteinase involved in the breakdown of casein. Enzyme specificity and profile of oligopeptide products produced is strain dependent. Proteinases from Lcb. paracasei (and Lcb. rhamnosus) are more suited for the salt and pH conditions in cheese, so they are less inhibited than lactococcal proteinases. When some strains are used as adjunct cultures, improved cheese flavor is usually accompanied by altered proteolysis leading to higher concentrations of amino acids and small peptides, and changes in the cheese peptide profile. Other strains can produce a bitter defect in cheese (Minervini and Calasso, 2020).
      In raw milk cheeses, NSLAB, especially heterofermentative lactobacilli such as the Lacticaseibacillus and Lactiplantibacillus, can grow from initial levels of 102 cfu/g during storage to levels 106 to 108 cfu/g in cheeses that have a warm ripening stage to promote growth and activity of propionibacteria (
      • Weinrichter B.
      • Sollberger H.
      • Ginzinger W.
      • Jaros D.
      • Rohm H.
      Adjunct starter properties affect characteristic features of Swiss-type cheeses.
      ). Often raw milk cheeses will vary in quality throughout the year as changes occur in the NSLAB population in the milk. To ensure the preferred NSLAB microbiota is present in the cheese, NSLAB can be isolated from good quality cheese and those strains used as an adjunct culture in future cheese production. Adding adjunct lactobacilli, even those derived from the NSLAB microbiota, above levels of 104 cfu/mL tends to produce atypical flavors during cheese ripening (
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      ).

      Lacticaseibacillus rhamnosus

      Lacticaseibacillus rhamnosus has a nomadic lifestyle being found in a broad range of habitats including dairy products, fermented meat, fish, vegetables and cereals, sewage, humans (oral, vaginal, and intestinal), invertebrate hosts and clinical sources (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Lacticaseibacillus rhamnosus is also used as an adjunct culture to prevent spoilage in dairy products (
      • Makki G.M.
      • Kozak S.M.
      • Jencarelli K.G.
      • Alcaine S.D.
      Evaluation of the efficacy of commercial protective cultures against mold and yeast in queso fresco.
      ).

      Companilactobacillus nodensis

      The genus Companilactobacillus refers to the association of Companilactobacillus species with other lactobacilli, particularly heterofermentative organisms, in cereal and vegetable fermentations (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Companilactobacillus nodensis was originally isolated from Japanese pickles (
      • Kashiwagi T.
      • Suzuki T.
      • Kamakura T.
      Lactobacillus nodensis sp. nov., isolated from rice bran.
      ) and has been detected in a Danish raw milk cheese where metabolically active bacteria during the ripening process were identified (
      • Masoud W.
      • Vogensen F.K.
      • Lillevang S.
      • Abu Al-Soud W.
      • Sørensen S.J.
      • Jakobsen M.
      The fate of indigenous microbiota, starter cultures, Escherichia coli, Listeria innocua and Staphylococcus aureus in Danish raw milk and cheeses determined by pyrosequencing and quantitative real time (qRT)-PCR.
      ). The species uses pentoses and hexoses, but not disaccharides, as carbon sources. The strain CSK964 was shown to produce volatile sulfur compounds including hydrogen sulfide. The strain was subsequently tested as a flavor adjunct in Gouda cheese, where hydrogen sulfide and methanethiol were present in higher abundances in cheeses containing the strain CSK964 of this species (
      • O'Brien E.
      • Mills S.
      • Dobson A.
      • Serrano L.M.
      • Hannon J.
      • Ryan S.P.
      • Kilcawley K.N.
      • Brandsma J.B.
      • Meijer W.C.
      • Hill C.
      • Ross R.P.
      Contribution of the novel sulfur-producing adjunct Lactobacillus nodensis to flavor development in Gouda cheese.
      ).

      Other Lactobacilli Isolated from Milk and Dairy Products

      Apart from the starter culture bacteria (L. lactis and S. thermophilus) lactobacilli comprise the majority of NSLAB present in cheese (
      • Overbeck S.L.
      Comparison of microbial diversity of fifteen aged Cheddar cheeses from different regions using next generation sequencing.
      ). Depending on the species and strain, their metabolic activity may contribute to defects or inconsistency in cheese quality and development of typical cheese flavor (
      • Blaya J.
      • Barzideh Z.
      • LaPointe G.
      Symposium review: Interaction of starter cultures and nonstarter lactic acid bacteria in the cheese environment.
      ). In Cheddar cheese, they are present initially at only 104 cfu/g or less but increase to 106 to 108 cfu/g within a few months (
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      ;
      • Blaya J.
      • Barzideh Z.
      • LaPointe G.
      Symposium review: Interaction of starter cultures and nonstarter lactic acid bacteria in the cheese environment.
      ). However, although the adjunct culture may initially dominate (e.g., 105 cfu/g compared with NSLAB numbers of typically ≤102 cfu/g in high quality cheese) with longer aging periods it is the wild type lactobacilli (lactobacilli not intentionally added to the milk) that dominate. In higher moisture cheese such as part skim Mozzarella or Scamorza cheese, this increase may occur within 1 mo (
      • Guidone A.
      • Braghieri A.
      • Cioffi S.
      • Claps S.
      • Genovese F.
      • Morone G.
      • Napolitano F.
      • Parente E.
      Effect of adjuncts on microbiological and chemical properties of Scamorza cheese.
      ). Lactobacilli are common contaminants of raw milk but generally make up only a small proportion of the raw milk microbiota ((Minervini and Calasso, 2020). Most do not survive pasteurization but some species such as Lacticaseibacillus paracasei ssp. tolerans can survive as well as some other strains of Lcb. paracasei which would be present in cheese milk at low levels.
      Initial numbers of NSLAB in cheese are influenced by their numbers in raw milk (especially if pasteurization is not used) and the extent of postpasteurization contamination from biofilm buildup in processing equipment and pipelines. The environment inside individual dairy factories becomes the permanent habitat for strains of lactobacilli that can differ from facility to facility. Such lactobacilli thus replace the heat-sensitive lactobacilli present in raw milk, and may impart individual flavor characteristics to cheese made in a particular factory (
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      ). The presence of such NSLAB in factories that produce high quality cheese appear to have a beneficial effect on generating good Cheddar cheese flavor during the aging process and these NSLAB isolates have been used as adjunct cultures to improve flavor development during ripening (
      • Reiter B.
      • Fryer T.F.
      • Sharpe M.E.
      A method of maintaining a reference flora of constant bacteriological composition.
      ;
      • Law B.A.
      • Castañón M.
      • Sharpe M.E.
      The effect of non-starter bacteria on flavor development in Cheddar cheese.
      ;
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      ;
      • Lynch C.M.
      • McSweeney P.L.H.
      • Fox P.F.
      • Cogan T.M.
      • Drinan F.D.
      Manufacture of Cheddar cheese with and without adjunct lactobacilli under controlled microbiological conditions.
      ).
      Numerous lactobacilli are also part of plant fermentations and have been isolated from silage use as feed (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). These organisms, although not used in dairy fermentations, are an important source of spoilage in dairy products. A list of some of these are given in Table 8. Many lactobacilli are also used as starter cultures for silage such as Lentilactobacillus species (e.g., Lentilactobacillus buchneri), which are then isolated from dairy products. Many other lactobacilli have been isolated from dairy products, but are not used as starters, adjuncts, or associated with dairy silage. These organisms originate from environmental sources and are listed in Table 9.
      Table 8Lactobacilli species isolated from silage (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      )
      GenusSpecies
      Lactobacillusacetotolerans, helsingborgensis, helveticus, taiwanensis
      Lacticaseibacilluscasei, paracasei ssp. paracasei, paracasei ssp. tolerans, manihotivorans, nasuensis
      Lactiplantibacillusplantarum ssp. plantarum, plantarum ssp. argentoratensis, pentosus
      Lapidilactobacillusdextrinicus
      Latilactobacilluscurvatus, graminis
      Lentilactobacillusbuchneri, diolivorans, hilgardii, parabuchneri, parafarraginis
      Levilactobacillusbrevis, hammesii
      Limosilactobacilluspontis
      Loigolactobacilluscoryniformis ssp. coryniformis, coryniformisssp. torquens, iwatensis, paraplantarum
      Amylolactobacillusamylotrophicus
      Paucilactobacillushokkaidonensis, suebicus, vaccinostercus, wasatchensis
      Companilactobacillus,farciminis, formosensis
      Secundilactobacillusmixtipabuli, pentosiphilus, silage, silagincola
      Table 9Other lactobacilli
      Genus abbreviations as described in Table 2.
      that have been associated with dairy foods
      Isolated speciesDairy productAttributeReference
      Lb. delbrueckii ssp. indicusIsolated from Dahi, a fermented dairy product from IndiaMetabolizes sucrose, fructose, lactose and mannose, but is unable to ferment maltose and trehalose
      • Dellaglio F.
      • Felis G.E.
      • Castioni A.
      • Torriani S.
      • Germond J.E.
      Lactobacillus delbrueckii subsp. indicus subsp. nov., isolated from Indian dairy products.
      Lb. sakeiIsolated from raw milk Oaxaca cheese in Mexico
      • Caro I.
      • Mateo J.
      • Sandoval M.H.
      • Soto S.
      • García-Armesto M.R.
      • Castro J.M.
      Characterization of Oaxaca raw milk cheese microbiota with particular interest in Lactobacillus strains.
      Lb. diolivoransIsolated from raw milk and cheese, kefir and maize silageHas high tolerance for solvents, and can produce 1,3 propanediol and 3-hydroxypropionate from glycerol, propanol and propionate from propanediol, and 2-butanol from meso-2,3-butanediol
      • Agostini C.
      • Eckert C.
      • Vincenzi A.
      • Machado B.L.
      • Jordon B.C.
      • Kipper J.P.
      • Dullius A.
      • Dullius C.H.
      • Lehn D.N.
      • Sperotto R.A.
      • Pozzobon A.
      • Granada C.E.
      • Maciel M.J.
      • Volken de Souza C.F.
      Characterization of technological and probiotic properties of indigenous Lactobacillus spp. from south Brazil.
      Abatemarco et al., 2018
      • Russmayer H.
      • Marx H.
      • Sauer M.
      Microbial 2-butanol production with Lactobacillus diolivorans..
      Lpb. paraplantarumPart of the starter culture used for Beyaz cheese production; isolated from ricotta forte cheese, Feta cheese and in Tahana, a traditional fermented Turkish product composed of spontaneously fermented yogurt and wheat flour product and in silageHomofermentative; produces lactic acid from glucose and also ferment lactose and galactose
      • Karahan A.G.
      • Başyiğit Kiliç G.
      • Kart A.
      • Aloğlu H.S.
      • Oner Z.
      • Aydemir S.
      • Erkuş O.
      • Harsa S.
      Genotypic identification of some lactic acid bacteria by amplified fragment length polymorphism analysis and investigation of their potential usage as starter culture combinations in Beyaz cheese manufacture.
      • Baruzzi F.
      • Morea M.
      • Matarante A.
      • Cocconcelli P.S.
      Changes in the Lactobacillus community during Ricotta forte cheese natural fermentation.
      • Manolopoulou E.
      • Sarantinopoulos P.
      • Zoidou E.
      • Aktypis A.
      • Moschopoulou E.
      • Kandarakis I.G.
      • Anifantakis E.M.
      Evolution of microbial populations during traditional Feta cheese manufacture and ripening.
      • Sengun I.Y.
      • Nielsen D.S.
      • Karapinar M.
      • Jakobsen M.
      Identification of lactic acid bacteria isolated from Tarhana, a traditional Turkish fermented food.
      • Pang H.
      • Qin G.
      • Tan Z.
      • Li Z.
      • Wang Y.
      • Cai Y.
      Natural populations of lactic acid bacteria associated with silage fermentation as determined by phenotype, 16S ribosomal RNA and recA gene analysis.
      Lpb. pentosusIsolated raw bovine milk, fermented goat's milk and Brazilian artisanal cheeseHomofermentative; produces lactic acid from glucose and also ferment lactose and galactose
      • Agostini C.
      • Eckert C.
      • Vincenzi A.
      • Machado B.L.
      • Jordon B.C.
      • Kipper J.P.
      • Dullius A.
      • Dullius C.H.
      • Lehn D.N.
      • Sperotto R.A.
      • Pozzobon A.
      • Granada C.E.
      • Maciel M.J.
      • Volken de Souza C.F.
      Characterization of technological and probiotic properties of indigenous Lactobacillus spp. from south Brazil.
      • Cho G.S.
      • Cappello C.
      • Schrader K.
      • Fagbemigum O.
      • Oguntoyinbo F.A.
      • Csovcsics C.
      • Rösch N.
      • Kabisch J.
      • Neve H.
      • Bockelmann W.
      • Briviba K.
      • Modesto M.
      • Cilli E.
      • Mattarelli P.
      • Franz C.M.A.P.
      Isolation and characterization of lactic acid bacteria from fermented goat milk in Tajikistan.
      Lat. curvatusPart of the nonstarter lactic acid bacteria microbiota of many cheeses and often the dominant lactobacilliLactic acid is produced from most hexoses and some pentoses and disaccharides; does not ferment xylose Can promote calcium lactate crystal formation
      • Broadbent J.R.
      • Houck K.
      • Johnson M.E.
      • Oberg C.J.
      Influence of adjunct use and cheese microenvironment on nonstarter bacteria in reduced-fat Cheddar-type cheese.
      • Chou Y.E.
      • Edwards C.G.
      • Luedecke L.O.
      • Bates M.P.
      • Clark S.
      Nonstarter lactic acid bacteria and aging temperature affect calcium lactate crystallization in cheddar cheese.
      Len. sunkiiIsolated from kefirHeterofermentative; produces gas from glucose; produces, both lactic acid
      • Han X.
      • Zhang L.J.
      • Wu H.Y.
      • Wu Y.F.
      • Zhao S.N.
      Investigation of microorganisms involved in kefir biofilm formation.
      Len. hilgardiiPrimarily associated with silage inoculation; found as part of the NSLAB population of white-brined cheeses made from goat's or sheep's milk
      • Ávila C.L.
      • Carvalho B.F.
      • Pinto J.C.
      • Duarte W.F.
      • Schwan R.F.
      The use of Lactobacillus species as starter cultures for enhancing the quality of sugar cane silage.
      .
      Len. kefiriIsolated from Camembert and ricotta forte cheeses and in raw camel milk
      • Baruzzi F.
      • Morea M.
      • Matarante A.
      • Cocconcelli P.S.
      Changes in the Lactobacillus community during Ricotta forte cheese natural fermentation.
      • Akhmetsadykova S.H.
      • Baubekova A.
      • Konuspayeva G.
      • Akhmetsadykov N.
      • Faye B.
      • Loiseau G.
      Lactic acid bacteria biodiversity in raw and fermented camel milk.
      Len. parakefiriA predominant lactic acid bacteria in butter purchased in Russia
      • Syromyatnikov M.Y.
      • Kokina A.V.
      • Solodskikh S.A.
      • Panevina A.V.
      • Popov E.S.
      • Popov V.N.
      High-throughput 16S rRNA gene sequencing of butter microbiota reveals a variety of opportunistic pathogens.
      Len. buchneriIsolated from milk, Swiss, Canestrato Pugliese and ricotta forte, kefir, and traditional fermented dairy products such qula and kurutAssociated with biogenic amine formation. Used as silage inoculant; can produce 1,2-propanediol from lactic acid
      • Sumner S.S.
      • Speckhard M.W.
      • Somers E.B.
      • Taylor S.L.
      Isolation of histamine-producing Lactobacillus buchneri from Swiss cheese implicated in a food poisoning outbreak.
      • Zhang B.
      • Wang Y.
      • Tan Z.
      • Li Z.
      • Jiao Z.
      • Huang Q.
      Screening of probiotic activities of lactobacilli strains isolated from traditional Tibetan Qula, a raw Yak milk cheese.
      • Sun Z.
      • Harris H.M.B.
      • McCann A.
      • Guo C.
      • Argimón S.
      • Zhang W.
      • Yang X.
      • Jeffery I.B.
      • Cooney J.C.
      • Kagawa T.F.
      • Liu W.
      • Song Y.
      • Salvetti E.
      • Wrobel A.
      • Rasinkangas P.
      • Parkhill J.
      • Rea M.C.
      • O'Sullivan O.
      • Ritari J.
      • Douillard F.P.
      • Paul Ross R.
      • Yang R.
      • Briner A.E.
      • Felis G.E.
      • de Vos W.M.
      • Barrangou R.
      • Klaenhammer T.R.
      • Caufield P.W.
      • Cui Y.
      • Zhang H.
      • O'Toole P.W.
      Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera.
      • Muck R.E.
      • Nadeau E.M.G.
      • McAllister T.A.
      • Contreras-Govea F.E.
      • Santos M.C.
      • Kung Jr., L.
      Silage review: Recent advances and future uses of silage additives.
      • Diaz M.
      • Del Rio B.
      • Sanchez-Llana E.
      • Ladero V.
      • Redruello B.
      • Fernández M.
      • Martin M.C.
      • Alvarez M.A.
      Histamine-producing Lactobacillus parabuchneri strains isolated from grated cheese can form biofilms on stainless steel.
      Len. parabuchneriIsolated from raw milk and artisanal cheeses, Camembert and Parmigiano Reggiano cheesesResponsible for accumulation of histamine in many cheeses; heterofermentative and forms CO2 from, hexoses.
      • Agostini C.
      • Eckert C.
      • Vincenzi A.
      • Machado B.L.
      • Jordon B.C.
      • Kipper J.P.
      • Dullius A.
      • Dullius C.H.
      • Lehn D.N.
      • Sperotto R.A.
      • Pozzobon A.
      • Granada C.E.
      • Maciel M.J.
      • Volken de Souza C.F.
      Characterization of technological and probiotic properties of indigenous Lactobacillus spp. from south Brazil.
      • Guarcello R.
      • De Angelis M.
      • Settanni L.
      • Formiglio S.
      • Gaglio R.
      • Minervini F.
      • Moschetti G.
      • Gobbetti M.
      Selection of amine-oxidizing dairy lactic acid bacteria and identification of the enzyme and gene involved in the decrease of biogenic amines.
      • Henri-Dubernet S.
      • Desmasures N.
      • Guéguen M.
      Diversity and dynamics of lactobacilli populations during ripening of RDO Camembert cheese.
      • Gala E.
      • Landi S.
      • Solieri L.
      • Nocetti M.
      • Pulvirenti A.
      • Giudici P.
      Diversity of lactic acid bacteria population in ripened Parmigiano Reggiano cheese.
      • Wüthrich D.
      • Berthoud H.
      • Wechsler D.
      • Eugster E.
      • Irmler S.
      • Bruggmann R.
      The histidine decarboxylase gene cluster of Lactobacillus parabuchneri was gained by horizontal gene transfer and is mobile within the species.
      • Vancanneyt M.
      • Naser S.M.
      • Engelbeen K.
      • De Wachter M.
      • Van der Meulen R.
      • Cleenwerck I.
      • Hoste B.
      • De Vuyst L.
      • Swings J.
      Reclassification of Lactobacillus brevis strains LMG 11494 and LMG 11984 as Lactobacillus parabrevis sp. nov.
      Len. otakiensisisolated from bovine raw milk and artisanal cheese from southern BrazilHeterofermentative; both lactic acid are produced, and gas is produced from glucose
      • Agostini C.
      • Eckert C.
      • Vincenzi A.
      • Machado B.L.
      • Jordon B.C.
      • Kipper J.P.
      • Dullius A.
      • Dullius C.H.
      • Lehn D.N.
      • Sperotto R.A.
      • Pozzobon A.
      • Granada C.E.
      • Maciel M.J.
      • Volken de Souza C.F.
      Characterization of technological and probiotic properties of indigenous Lactobacillus spp. from south Brazil.
      Lev. brevisIsolated from Cheddar cheese, many artisanal dairy products and in raw camel's milkSome strains produce high levels of γ-aminobutyric acid; heterofermentative
      • Fitzsimons N.A.
      • Cogan T.M.
      • Condon S.
      • Beresford T.
      Phenotypic and genotypic characterization of non-starter lactic acid bacteria in mature cheddar cheese.
      • Gantzias C.
      • Lappa I.K.
      • Aerts M.
      • Georgalaki M.
      • Manolopoulou E.
      • Papadimitriou K.
      • De Brandt E.
      • Tsakalidou E.
      • Vandamme P.
      MALDI-TOF MS profiling of non-starter lactic acid bacteria from artisanal cheeses of the Greek island of Naxos.
      • Sokovic Bajic S.
      • Djokic J.
      • Dinic M.
      • Veljovic K.
      • Golic N.
      • Mihajlovic S.
      • Tolinacki M.
      GABA-producing natural dairy isolate from artisanal Zlatar cheese attenuates gut inflammation and strengthens gut epithelial barrier in vitro..
      • Carafa I.
      • Stocco G.
      • Nardin T.
      • Larcher R.
      • Bittante G.
      • Tuohy K.
      • Franciosi E.
      Production of naturally γ-aminobutyric acid-enriched cheese using the dairy strains Streptococcus thermophilus 84C and Lactobacillus brevis DSM 32386.
      • Derriche I.
      • Nogacka A.M.
      • Salazar N.
      • Ruas-Madiedo P.
      • Gueimonde M.
      • Bensalah F.
      • de Los Reyes-Gavilán C.G.
      Effect of inulin-type fructans and galactooligosaccharides on cultures of Lactobacillus strains isolated in Algeria from camel's milk and human colostrum.
      Lev. parabrevisOriginally isolated from a farmhouse red Cheshire cheeseHeterofermentative and produces CO2 from glucose and gluconate
      • Vancanneyt M.
      • Naser S.M.
      • Engelbeen K.
      • De Wachter M.
      • Van der Meulen R.
      • Cleenwerck I.
      • Hoste B.
      • De Vuyst L.
      • Swings J.
      Reclassification of Lactobacillus brevis strains LMG 11494 and LMG 11984 as Lactobacillus parabrevis sp. nov.
      Lev. angrenensisIsolated from traditional yogurt in TibetHeterofermentative; ferments and produces gas from glucose; ferments galactose but not from lactose
      • Long G.Y.
      • Wei X.Y.
      • Tu W.
      • Gu C.T.
      Lactobacillus hegangensis sp. nov., Lactobacillus suibinensis sp. nov., Lactobacillus daqingensis sp. nov., Lactobacillus yichunensis sp. nov., Lactobacillus mulanensis sp. nov., Lactobacillus achengensis sp. nov., Lactobacillus wuchangensis sp. nov., Lactobacillus gannanensis sp. nov., Lactobacillus binensis sp. nov. and Lactobacillus angrenensis sp. nov., isolated from Chinese traditional pickle and yogurt.
      Lig. agilisIsolated from traditional Iranian cheesesAcid is produced from glucose, galactose and lactose with weak reaction on pentoses
      • Ehsani A.
      • Hashemi M.
      • Afshari A.
      • Aminzare M.
      Probiotic white cheese production using coculture with Lactobacillus species isolated from traditional cheeses.
      • Baele M.
      • Devriese L.A.
      • Haesebrouck F.
      Lactobacillus agilis is an important component of the pigeon crop flora.
      Lig. acidipiscisIsolated from Mexican cheeses such as Cotija and double cream Chiapas cheese and traditional Greek Kopanisti cheese as well as silageHomofermentative, and halotolerant, produces lactic acid from glucose; contributes to the volatile flavor compounds in cheese
      • Morales F.
      • Morales J.I.
      • Hernández C.H.
      • Hernández-Sánchez H.
      Isolation and partial characterization of halotolerant lactic acid bacteria from two Mexican cheeses.
      • Kazou M.
      • Alexandraki V.
      • Blom J.
      • Pot B.
      • Tsakalidou E.
      • Papadimitriou K.
      Comparative genomics of Lactobacillus acidipiscis ACA-DC 1533 isolated from traditional Greek Kopanisti cheese against species within the Lactobacillus salivarius clade.
      Lim. pontisIsolated from a raw milk Piedmont cheese made from raw milk and corn silage
      • Bautista-Gallego J.
      • Alessandria V.
      • Fontana M.
      • Bisotti S.
      • Taricco S.
      • Dolci P.
      • Cocolin L.
      • Rantsiou K.
      Diversity and functional characterization of Lactobacillus spp. isolated throughout the ripening of a hard cheese.
      • Han H.
      • Ogata Y.
      • Yamamoto Y.
      • Nagao S.
      • Nishino N.
      Identification of lactic acid bacteria in the rumen and feces of dairy cows fed total mixed ration silage to assess the survival of silage bacteria in the gut.
      Lim. fermentumRagusano and Manchego cheesesHeterofermenter with sugar fermentation being strain dependent
      • Randazzo C.L.
      • Torriani S.
      • Akkermans A.D.
      • de Vos W.M.
      • Vaughan E.E.
      Diversity, dynamics, and activity of bacterial communities during production of an artisanal Sicilian cheese as evaluated by 16S rRNA analysis.
      • Sánchez I.
      • Seseña S.
      • Poveda J.M.
      • Cabezas L.
      • Palop L.
      Genetic diversity, dynamics, and activity of Lactobacillus community involved in traditional processing of artisanal Manchego cheese.
      • Dellaglio F.
      • Torriani S.
      • Felis G.E.
      Reclassification of Lactobacillus cellobiosus Rogosa et al. 1953 as a later synonym of Lactobacillus fermentum Beijerinck 1901.
      Lo. renniniIsolated from calf rennet; associated with cheese spoilage and isolated from a traditional Greek overripened Kopanisti cheese called ManaHomofermentative, no gas is produced from glucose or gluconate produces lactic acid
      • Chenoll E.
      • Macián M.C.
      • Aznar R.
      Lactobacillus rennini sp. nov., isolated from rennin and associated with cheese spoilage.
      • Kazou M.
      • Alexandraki V.
      • Blom J.
      • Pot B.
      • Tsakalidou E.
      • Papadimitriou K.
      Comparative genomics of Lactobacillus acidipiscis ACA-DC 1533 isolated from traditional Greek Kopanisti cheese against species within the Lactobacillus salivarius clade.
      Lo. bifermentansCauses small cracks and gas formation in Edam and Gouda; isolated from Himalayan fermented milksHeterofermentative with end lactic acid, acetic acid, ethanol, traces of propionic acid, carbon dioxide and free H2 as some of the end products of fermentation
      • Kandler O.
      • Schillinger U.
      • Weiss N.
      Lactobacillus bifermentans sp. nov., nom. rev., an organism forming CO(2) and H(2) from lactic acid.
      • Dewan S.
      • Tamang J.P.
      Dominant lactic acid bacteria and their technological properties isolated from the Himalayan ethnic fermented milk products.
      Lo. coryniformisIsolated goat's milk cheese, Castelmagno cheese, Feta cheese, silage and cow dungLo. coryniformis ssp. coryniformis produces lactic acid from glucose
      • Martín R.
      • Olivares M.
      • Marín M.L.
      • Xaus J.
      • Fernández L.
      • Rodríguez J.M.
      Characterization of a reuterin-producing Lactobacillus coryniformis strain isolated from a goat's milk cheese.
      • Dolci P.
      • Alessandria V.
      • Rantsiou K.
      • Rolle L.
      • Zeppa G.
      • Cocolin L.
      Microbial dynamics of Castelmagno PDO, a traditional Italian cheese, with a focus on lactic acid bacteria ecology.
      • Rantsiou K.
      • Urso R.
      • Dolci P.
      • Comi G.
      • Cocolin L.
      Microflora of Feta cheese from four Greek manufacturers.
      • Wu J.J.
      • Du R.P.
      • Gao M.
      • Sui Y.Q.
      • Xiu L.
      • Wang X.
      Naturally occurring lactic acid bacteria isolated from tomato pomace silage.
      Co. zhongbaensisIsolated from a Tibetian yogurtHomofermentative; ferments glucose, lactose and galactose
      • Wei Y.X.
      • Gu C.T.
      Lactobacillus yilanensis sp. nov., Lactobacillus bayanensis sp. nov., Lactobacillus keshanensis sp. nov., Lactobacillus kedongensis sp. nov., Lactobacillus baiquanensis sp. nov., Lactobacillus jidongensis sp. nov., Lactobacillus hulinensis sp. nov., Lactobacillus mishanensis sp. nov. and Lactobacillus zhongbaensis sp. nov., isolated from Chinese traditional pickle and yogurt.
      Sc. shenzhenensisIsolated from a fermented dairy beverage in ChinaHeterofermentative species; ferments lactose and galactose but not glucose
      • Zou Y.
      • Liu F.
      • Fang C.
      • Wan D.
      • Yang R.
      • Su Q.
      • Yang R.
      • Zhao J.
      Lactobacillus shenzhenensis sp. nov., isolated from a fermented dairy beverage.
      Se. collinoidesIsolated from traditional Iranian dairy products
      • Karami S.
      • Roayaei M.
      • Hamzavi H.
      • Bahmani M.
      • Hassansad-Azar H.
      • Leila M.
      • Rafieian-Kopaei M.
      Isolation and identification of probiotic Lactobacillus from local dairy and evaluating their antagonistic effect on pathogens.
      Co. crustorumFirst isolated from koumiss; also isolated from raw bovine milk and traditional Iranian dairy productsβ-glucuronidase activity observed in some strains; cannot ferment pentoses; disaccharide fermentation is strain dependent
      • Danova S.
      • Petrov K.
      • Pavlov P.
      • Petrova P.
      Isolation and characterization of Lactobacillus strains involved in koumiss fermentation.
      • Yi L.
      • Dang Y.
      • Wu J.
      • Zhang L.
      • Liu X.
      • Liu B.
      • Zhou Y.
      • Lu X.
      Purification and characterization of a novel bacteriocin produced by Lactobacillus crustorum MN047 isolated from koumiss from Xinjiang, China.
      • Qian B.
      • Yin L.
      • Yao X.
      • Zhong Y.
      • Gui J.
      • Lu F.
      • Zhang F.
      • Zhang J.
      Effects of fermentation on the hemolytic activity and degradation of Camellia oleifera saponins by Lactobacillus crustorum and Bacillus subtilis..
      • Sharafi H.
      • Derakhshan V.
      • Paknejad M.
      • Alidoust L.
      • Tohidi A.
      • Pornour M.
      • Hajfarajollah H.
      • Zahiri H.S.
      • Noghabi K.A.
      Lactobacillus crustorum KH: Novel prospective probiotic strain isolated from Iranian traditional dairy products.
      Pa. wasatchensisIsolated from gassy Cheddar cheesesUses ribose to support growth and produces CO2
      • Oberg C.J.
      • Oberg T.S.
      • Culumber M.D.
      • Ortakci F.
      • Broadbent J.R.
      • McMahon D.J.
      Lactobacillus wasatchensis sp. nov., a non-starter lactic acid bacteria isolated from aged Cheddar cheese.
      • Culumber M.
      • McMahon D.J.
      • Ortakci F.
      • Montierth L.
      • Villalba B.
      • Broadbent J.
      • Oberg C.J.
      Geographical distribution and strain diversity of Lactobacillus wasatchensis isolated from cheese with unwanted gas formation.
      • McMahon D.J.
      • Bowen I.B.
      • Green I.
      • Domek M.
      • Oberg C.J.
      Growth and survival characteristics of Paucilactobacillus wasatchensis WDCO4.
      1 Genus abbreviations as described in Table 2.

      Lactiplantibacillus plantarum

      The genus Lactiplantibacillus is the previous plantarum-group lactobacilli with the name referring to their association with both milk and plants (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ). Lactiplantibacillus plantarum is a dominant member of the microbiota in spontaneous vegetable and olive fermentations, and also occurs in sourdough, dairy fermentations, and fermented meats. It can also be isolated from the human intestinal tract, including the oral cavity (
      • Zheng J.
      • Wittouck S.
      • Salvetti E.
      • Franz C.
      • Harris H.
      • Mattarelli P.
      • O'Toole P.W.
      • Pot B.
      • Vandamme P.
      • Walter J.
      • Watanabe K.
      • Wuyts S.
      • Felis G.E.
      • Gänzle M.G.
      • Lebeer S.
      A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae..
      ).
      From the 1930s until recently (Table 6) a dominant NSLAB isolated from cheese in New Zealand, the United Kingdom and the United States was Lpb. plantarum (
      • Peterson S.D.
      • Marshall R.T.
      Nonstarter lactobacilli in Cheddar cheese: A review.
      ;
      • Williams A.G.
      • Banks J.M.
      Proteolytic and other hydrolytic enzyme activities in non-starter lactic acid bacteria (NSLAB) isolated from Cheddar cheese manufactured in the United Kingdom.
      ). In the traditional manufacture of Oaxaca cheese in Mexico, raw milk is used without any starter culture addition (
      • De Oca-Flores E.M.
      • Castelán-Ortega O.A.
      • Estrada-Flores J.G.
      • Espinoza-Ortega A.
      Oaxaca cheese: Manufacture process and physicochemical characteristics.
      ) and the predominant lactobacilli isolated from such cheeses are various strains of Lpb. plantarum (
      • Caro I.
      • Mateo J.
      • Sandoval M.H.
      • Soto S.
      • García-Armesto M.R.
      • Castro J.M.
      Characterization of Oaxaca raw milk cheese microbiota with particular interest in Lactobacillus strains.
      ).
      Likewise, when strains of Lpb. plantarum (with broad-spectrum antibacterial activity in fermented milk) were added to yogurt, differences in volatile flavor compounds (such as 2,3-pentanedione, acetaldehyde and acetate) and texture were noted (
      • Li C.
      • Song J.
      • Kwok L.-Y.
      • Wang J.
      • Dong Y.
      • Yu H.
      • Hou Q.
      • Zhang H.
      • Chen Y.
      Influence of Lactobacillus plantarum on yogurt fermentation properties and subsequent changes during postfermentation storage.
      ). Several Lpb. plantarum EPS-producing strains have been isolated from various fermented foods as well as from kefir (
      • Wang X.
      • Xiao J.
      • Jia Y.
      • Pan Y.
      • Wang Y.
      Lactobacillus kefiranofaciens, the sole dominant and stable bacterial species, exhibits distinct morphotypes upon colonization in Tibetan kefir grains.
      ).

      Lactiplantibacillus paraplantarum

      Lactiplantibacillus paraplantarum is mostly associated with beer spoilage and vegetable fermentations, but can be found as part of the starter culture used for Beyaz cheese production (
      • Karahan A.G.
      • Başyiğit Kiliç G.
      • Kart A.
      • Aloğlu H.S.
      • Oner Z.
      • Aydemir S.
      • Erkuş O.
      • Harsa S.
      Genotypic identification of some lactic acid bacteria by amplified fragment length polymorphism analysis and investigation of their potential usage as starter culture combinations in Beyaz cheese manufacture.
      ), and as part of the microbiota in ricotta forte cheese (
      • Baruzzi F.
      • Morea M.
      • Matarante A.
      • Cocconcelli P.S.
      Changes in the Lactobacillus community during Ricotta forte cheese natural fermentation.
      ), in Feta cheese (
      • Manolopoulou E.
      • Sarantinopoulos P.
      • Zoidou E.
      • Aktypis A.
      • Moschopoulou E.
      • Kandarakis I.G.
      • Anifantakis E.M.
      Evolution of microbial populations during traditional Feta cheese manufacture and ripening.
      ), and in Tahana, a traditional fermented Turkish product composed of spontaneously fermented yogurt and wheat flour (
      • Sengun I.Y.
      • Nielsen D.S.
      • Karapinar M.
      • Jakobsen M.
      Identification of lactic acid bacteria isolated from Tarhana, a traditional Turkish fermented food.
      ) and in silage (
      • Pang H.
      • Qin G.
      • Tan Z.
      • Li Z.
      • Wang Y.
      • Cai Y.
      Natural populations of lactic acid bacteria associated with silage fermentation as determined by phenotype, 16S ribosomal RNA and recA gene analysis.
      ). A homofermentative species, they produce lactic acid from glucose. Researchers have experimented with purposely adding these bacteria isolated from nondairy sources into cheese with the aim of modifying flavor (
      • Ciocia F.
      • McSweeney P.L.H.
      • Piraino P.
      • Parente E.
      Use of dairy and no-dairy Lactobacillus plantarum, Lactobacillus paraplantarum, Lactobacillus pentosus strains as adjunct in Cheddar cheese.
      ). All strains ferment lactose and galactose (
      • Curk M.C.
      • Hubert J.C.
      • Bringel F.
      Lactobacillus paraplantarum sp. now., a new species related to Lactobacillus plantarum..
      ).

      Latilactobacillus curvatus

      The name of the genus Latilactobacillus refers to the bacteria having a widespread range of habitats, which is the case for Lat. curvatus, which has been isolated from a wide variety of environments including milk, cheese, fermented meat, fish and vegetable products, honey, corn and grass silage, and cow dung among others (
      • Torriani S.
      • Van Reenen G.A.
      • Klein G.
      • Reuter G.
      • Dellaglio F.
      • Dicks L.M.
      Lactobacillus curvatus subsp. curvatus subsp. nov. and Lactobacillus curvatus subsp. melibiosus subsp. nov. and Lactobacillus sake subsp. sake subsp. nov. and Lactobacillus sake subsp. carnosus subsp. nov., new subspecies of Lactobacillus curvatus Abo-Elnaga and Kandler 1965 and Lactobacillus sake Katagiri, Kitahara, and Fukami 1934 (Klein et al. 1996, emended descriptions), respectively.
      ;
      • Terán L.C.
      • Coeuret G.
      • Raya R.
      • Zagorec M.
      • Champomier-Vergès M.C.
      • Chaillou S.
      Phylogenomic analysis of Lactobacillus curvatus reveals two lineages distinguished by genes for fermenting plant-derived carbohydrates.
      ). Lactic acid is produced from the fermentation of most hexoses and some pentoses, but it cannot ferment xylose. It is a member of the NSLAB population of many cheese varieties and can grow to high numbers in hard and semi-hard cheeses, especially in Cheddar, Emmental, and Gruyère. Indeed, the organism is now the most common NSLAB found in cheese in North America (Broadbent et el., 2003). The species has been shown to be associated with gas-related defects (
      • Porcellato D.
      • Johnson M.E.
      • Houck K.
      • Skeie S.B.
      • Mills D.A.
      • Kalanetra K.M.
      • Steele J.L.
      Potential of Lactobacillus curvatus LFC1 to produce slits in Cheddar cheese.
      ) and an increase in calcium lactate crystal formation (
      • Chou Y.E.
      • Edwards C.G.
      • Luedecke L.O.
      • Bates M.P.
      • Clark S.
      Nonstarter lactic acid bacteria and aging temperature affect calcium lactate crystallization in cheddar cheese.
      ) in Cheddar cheese and with the production of biogenic amines (
      • Barbieri F.
      • Montanari C.
      • Gardini F.
      • Tabanelli G.
      Biogenic amine production by lactic acid bacteria: A review.
      ). Other strains have shown probiotic potential as feed additives (
      • Hong S.W.
      • Kim J.H.
      • Bae H.J.
      • Ham J.S.
      • Yoo J.G.
      • Chung K.S.
      • Oh M.H.
      Selection and characterization of broad-spectrum antibacterial substance-producing Lactobacillus curvatus PA40 as a potential probiotic for feed additives.
      ).
      In a study using strains of Lcb. casei, Lcb. paracasei, Lpb. plantarum, and Lat. curvatus isolated from a good quality raw milk Cheddar cheese, the cheese made with Lcb. paracasei or Lpb. plantarum produced cheeses with the best flavor (
      • Lynch C.M.
      • McSweeney P.L.H.
      • Fox P.F.
      • Cogan T.M.
      • Drinan F.D.
      Manufacture of Cheddar cheese with and without adjunct lactobacilli under controlled microbiological conditions.
      ). Interestingly, strains of both of these species of lactobacilli died off during storage whereas the Lcb. casei and Lat. curvatus persisted at high numbers during storage.

      Lentilactobacillus buchneri

      This species has been isolated from milk, some cheese varieties including Swiss-type cheese (
      • Sumner S.S.
      • Speckhard M.W.
      • Somers E.B.
      • Taylor S.L.
      Isolation of histamine-producing Lactobacillus buchneri from Swiss cheese implicated in a food poisoning outbreak.
      ), Canestrato Pugliese and ricotta forte, kefir, and traditional fermented dairy products such as qula (
      • Zhang B.
      • Wang Y.
      • Tan Z.
      • Li Z.
      • Jiao Z.
      • Huang Q.
      Screening of probiotic activities of lactobacilli strains isolated from traditional Tibetan Qula, a raw Yak milk cheese.
      ) and kurut (
      • Sun Z.
      • Liu W.
      • Zhang J.
      • Yu J.
      • Zhang W.
      • Cai C.
      • Menghe B.
      • Sun T.
      • Zhang H.
      Identification and characterization of the dominant lactobacilli isolated from koumiss in China.
      ), and is used as a silage inoculant (
      • Muck R.E.
      • Nadeau E.M.G.
      • McAllister T.A.
      • Contreras-Govea F.E.
      • Santos M.C.
      • Kung Jr., L.
      Silage review: Recent advances and future uses of silage additives.