Advertisement
Article| Volume 84, ISSUE 6, P1294-1309, June 2001

Invited Review: Adhesion Mechanisms of Rumen Cellulolytic Bacteria

Open ArchiveDOI:https://doi.org/10.3168/jds.S0022-0302(01)70159-2
Invited Review: Adhesion Mechanisms of Rumen Cellulolytic Bacteria
Previous ArticleReproductive Loss in High-Producing Dairy Cattle: Where Will It End?
Next ArticleColloidal Calcium Phosphates in Casein Micelles Studied by Slow-Speed-Spinning 31P Magic Angle Spinning Solid-State Nuclear Magnetic Resonance
      This paper is only available as a PDF. To read, Please Download here.

      Abstract

      We divided the adhesion process of the predominant cellulolytic rumen bacteria Fibrobacter succinogenes, Ruminococcus flavefaciens, and Ruminococcus albus into four phases: 1) transport of the nonmotile bacteria to the substrate; 2) initial nonspecific adhesion of bacteria to unprotected sites of the substrate that is dominated by constitutive elements of bacterial glycocalyx; 3) specific adhesion via adhesins or ligands formation with the substrate, which can be dominated by several bacterial organelles including cellulosome complexes, fimbriae connections, glycosylated epitopes of cellulose-binding protein (CBP) or glycocalyx, and cellulose-binding domain (CBD) of enzymes; 4) proliferation of the attached bacteria on potentially digestible tissues of the substrate. Each of the phases and its significance in the adhesion process are described. Factors affecting bacterial adhesion are described including: 1) factors related to bacterial age, glycocalyx condition, and microbial competition; 2) factors related to the nature of substrate including, cuticle protection, surface area, hydration, and ionic charge; and 3) environmental factors including pH, temperature, and presence of cations and soluble carbohydrate. Based on the information available from the literature, it appears that each of the predominant rumen bacteria—F. succinogenes, R. flavefaciens, and R. albus—has a specific mechanism of adhesion to cellulose. In F. succinogenes, both the glycosidic residues of the outer membrane CBP and especially of the 180-kDa CBP, and the distinct CBD of EG2 EGF and Cl-stimulated cellobiosidase, may play a role in the adhesion to cellulose. No direct evidence, except scanning electron microscopy observations, yet supports the existence of either cellulosome complex or fimbriae structures involved in the adhesion mechanism of F. succinogenes. At least two mechanisms, cellulosome-like complexes and carbohydrate epitopes of the glycocalyx layer are involved in the specific adhesion of R. flavefaciens to cellulose. Ruminococcus albus possesses at least two mechanisms for specific adhesion to cellulose: a cellulosomal-like mechanism, and a CbpC (Pil)-protein mechanism that probably involves the production of fimbrial-like structures. Indirect and direct studies suggested that carbohydrate epitopes of CBPs and CBD epitope of cellulases may also be involved mostly in the nonspecific phase of adhesion of R. albus.

      Key words

      References

        • Akin D.E.
        Microscopic evaluation of forage digestion by rumen microorganisms—A review.
        J. Anim. Sci. 1979; 48: 701-710
        • Akin D.E.
        Histological and physical factors affecting digestibility of forages.
        Agron. J. 1989; 81: 17-23
        • Anacker R.L.
        • List R.H.
        • Mann R.E.
        • Hayes S.F.
        • Thomas L.A.
        Characterisation of monoclonal antibodies protecting mice against Rickettsia rickettsii.
        J. Infect. Dis. 1985; 151: 1052-1060
        • Baintner K.
        • Duncan S.H.
        • Stewart C.S.
        • Pusztai A.
        Binding and degradation of lectins by components of rumen liquor.
        J. Appl. Bacteriol. 1993; 74: 29-35
        • Bauchop T.
        Scanning electron microscopy in the study of microbial digestion of plant fragments in the gut.
        in: Elwood D.C. Hedger J.N. Latham M.J. Lynchand J.M. Slater J.H. Contemporary Microbial Ecology. Academic Press, New York, NY1980: 101-110
        • Bayer E.A.
        • Shimon L.J.W.
        • Lamed R.
        • Shoham Y.
        Cellulosomes: structure and ultrastructure.
        J. Struct. Biol. 1998; 124: 221-234
        • Bayer E.A.
        • Ding S.Y.
        • Shoham Y.
        • Lamed R.
        New perspectives in the structure of cellulosome-related domains from different species.
        in: Ohmiya K. Hayashi K. Sakka K. Kobayashi Y. Karita S. Kimura T. Genetics, Biochemistry and Ecology of Cellulose Degradation. Uni Publishers, Tokyo, Japan1999: 428-436
        • Beguin P.
        • Lemaire M.
        The cellulosome: an exocellular, multiprotein complex specialized in cellulose degradation.
        Crit. Rev. Biochem. Mol. Biol. 1996; 31: 201-236
        • Ben-Ghedalia D.
        • Miron J.
        • Solomon R.
        The degradation and utilization of structural polysaccharides of sorghum straw by defined ruminal bacteria.
        Anim. Feed Sci. Technol. 1993; 42: 283-295
        • Bera C.
        • Gaudet G.
        • Forano E.
        Regulation of glycosyl-hydrolase genes expression in Fibrobacter succinogenes S85.
        in: Ohmiya K. Hayashi K. Sakka K. Kobayashi Y. Karita S. Kimura T. Genetics, Biochemistry and Ecology of Cellulose Degradation. Uni Publishers, Tokyo, Japan1999: 541-544
        • Bhat S.
        • Wallce R.J.
        • Orskov E.R.
        Adhesion of cellulolytic ruminal bacteria to barley straw.
        Appl. Environ. Microbiol. 1990; 56: 2698-2703
        • Blair B.G.
        • Anderson K.L.
        Comparison of staining techniques for scanning electron microscopic detection of ultrastructural protuberances on cellulolytic bacteria.
        Biotech. Histochem. 1998; 73: 107-113
        • Busscher H.J.
        • Weerkamp A.H.
        Specific and non-specific interactions in bacterial adhesion to solid substrate.
        FEMS Microbiol. Rev. 1987; 46: 165-174
        • Chan W.W.
        • Dehority B.A.
        Production of Ruminococcus flavefaciens growth inhibitors by Ruminococcus albus.
        Anim. Feed Sci. Technol. 1999; 77: 61-71
        • Cheng K.H.
        • Akin D.E.
        • Costerton J.W.
        Rumen bacteria: Interaction with particulate dietary components and response to dietary variation.
        Fed. Proc. 1977; 36: 193-203
        • Cheng K.J.
        • Costerton J.W.
        Adhesive bacteria—Their role in the digestion of plant material, urea and ephithelial cells.
        in: Ruckebusch Y. Thivend P. Digestive Physiology and Metabolism in Ruminants. MTP press Ltd., Lancaster, England1980: 225-250
        • Cheng K.J.
        • Stewart C.S.
        • Dinsdale D.
        • Costerton J.W.
        Electron microscopy of bacteria involved in the digestion of plant cell walls.
        Anim. Feed Sci. Technol. 1983; 10: 93-120
        • Costerton J.W.
        • Irvin R.T.
        • Cheng K.J.
        The bacterial glycocalyx in nature and disease.
        Annu. Rev. Microbiol. 1981; 35: 299-324
        • Craig W.M.
        • Broderick G.A.
        • Ricker D.B.
        Quantitation of microorganisms associated with the particulate phase of ruminal ingesta.
        J. Nutr. 1987; 117: 56-64
        • Din N.
        • Gilkes N.R.
        • Tekant B.
        • Miller R.C.
        • Anthony R.
        • Warren J.
        • Kilburn D.G.
        Non-hydrolytic disruption of cellulose fibres by the binding domain of a bacterial cellulase.
        Biotechnology. 1991; 9: 1096-1099
        • Dinsdale D.
        • Morris E.J.
        • Bacon J.S.D.
        Electron microscopy of the microbial populations present and their modes of attack on various cellulosic substrates undergoing digestion in the sheep rumen.
        Appl. Environ. Microbiol. 1978; 36: 160-168
        • Doerner K.C.
        • Howard G.T.
        • Mackie R.I.
        • White B.A.
        β-Glucanase expression by Ruminococcus flavefaciens FD-1.
        FEMS Microbiol. Lett. 1992; 93: 147-154
        • Doyle R.J.
        • Sonnenfeld E.M.
        Properties of the cell surfaces of pathogenic bacteria.
        Int. Rev. Cytol. 1989; 118: 33-92
        • Fenno J.C.
        • Leblanc D.J.
        • Fives-taylor P.
        Nucleotide sequence analysis of a type I fimbrial gene of Streptococcus sanguis FW213.
        Infec. Immun. 1989; 57: 3527-3533
        • Fives-Taylor P.M.
        • Thompson D.W.
        Surface properties of Streptococcus sanguis FW213 mutants nonadherent to saliva-coated hydroxyapatite.
        Infect. Immun. 1985; 47: 752-759
        • Flint H.J.
        • Aurilia V.
        • Kirby J.
        • Miyazaki K.
        • Rincon-Torres M.T.
        • McCrae S.I.
        • Martin J.C.
        Organization of plant cell wall degrading enzymes in the ruminal anaerobic bacteria Ruminococcus flavefaciens and Prevotella bryantii.
        in: Ohmiya K. Hayashi K. Sakka K. Kobayashi Y. Karita S. Kimura T. Genetics, Biochemistry and Ecology of Cellulose Degradation. Uni Publishers, Tokyo, Japan1999: 511-519
        • Forsberg C.W.
        • Gong J.
        • Malburg L.M.J.
        • Zhu H.
        • Iyo A.
        • Cheng K.J.
        • Krell P.J.
        • Phillips J.P.
        Cellulases and hemicellulases of Fibrobacter succinogenes and their roles in fibre digestion.
        in: Shimada K. Hoshino S. Ohmiya K. Sakka K. Kobayashiand Y. Karita S. Genetics, Biochemistry and Ecology of Lignocellulose Degradation. Uni Publishers Co., Ltd, Tokyo, Japan1993: 125-136
        • Forsberg C.W.
        • Lam R.
        Use of adenosine-5-triphosphate as an indicator of the microbial biomass in rumen contents.
        Appl. Environ. Microbiol. 1977; 33: 528-534
        • Gong J.
        • Egosimba E.E.
        • Forsberg C.W.
        Cellulose binding proteins of Fibrobacter succinogenes and the possible role of a 180-kDa cellulose binding glycoprotein in adhesion to cellulose.
        Can. J. Microbiol. 1996; 42: 453-460
        • Gong J.
        • Forsberg C.W.
        Factors affecting adhesion of Fibrobacter succinogenes S85 and adherence defective mutants to cellulose.
        Appl. Environ. Microbiol. 1989; 55: 3039-3044
        • Hobbs M.
        • Mattick J.S.
        Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes.
        Mol. Microbiol. 1993; 10: 233-243
        • Huang L.
        • Forsberg C.W.
        • Thomas D.Y.
        Purification and characterization of a chloride-stimulated cellobiosidase from Bacteroides succinogenes S85.
        J. Bacteriol. 1988; 170: 2923-2932
        • Iyo A.H.
        • Forsberg C.W.
        Endoglucanase G from Fibrobacter succinogenes S85 belongs to a class of enzymes characterized by a basic C-terminal domain.
        Can. J. Microbiol. 1996; 42: 934-943
        • Joblin K.N.
        Interactions between ruminal fibrolytic bacteria and fungi.
        in: Onodera R. Itabashi H. Ushida K. Yano H. Sasaki Y. Rumen Microbes and Digestive Physiology in Ruminants. Japan Scientific Societies Press, Tokyo, Japan1997: 3-10
        • Karita S.
        • Sakka K.
        • Ohmiya K.
        Cellulosomes and cellulase complexes of anaerobic microbes: their structure, models and function.
        in: Onodera R. Itabashi H. Ushida K. Yano H. Sasaki Y. Rumen Microbes and Digestive Physiology in Ruminants. Japan Scientific Societies Press, Tokyo1997: 47-57
        • Kim Y.S.
        • Wi S.G.
        • Myung K.H.
        Ultrastructural studies of a Ruminococcus albus surface structures involved in lignocellu-lose degradation.
        in: Ohmiya K. Hayashi K. Sakka K. Kobayashi Y. Karita S. Kimura T. Genetics, Biochemistry and Ecology of Cellulose Degradation. Uni Publishers, Tokyo, Japan1999: 531-540
        • Kirby J.
        • Martin J.
        • Daniel A.
        • Flint H.J.
        Dockerin-like sequences in cellulases and xylanases from the rumen cellulolytic bacterium Ruminococcus flavefaciens.
        FEMS Microbiol. Lett. 1997; 149: 213-219
        • Kudo H.
        • Cheng K.J.
        • Costerton J.W.
        Electron microscopy study of the methyl-cellulose mediated detachment of cellulolytic rumen bacteria from cellulose fibers.
        Can. J. Microbiol. 1987; 33: 267-272
        • Lamed R.
        • Setter E.
        • Kenig R.
        • Bayer E.A.
        The cellulosome a discrete cell surface organelle of Clostridium thermocellum which exhibits separate antigenic, cellulose-binding, and various cellulolytic activities.
        Biotechnol. Bioeng. 1983; 13: 163-181
        • Lamed R.
        • Naimark J.
        • Morgenstern E.
        • Bayer E.A.
        Specialized cell surface structures in cellulolytic bacteria.
        J. Bacteriol. 1987; 169: 3792-3800
        • Larson M.A.
        • Heng N.C.K.
        • Morrison M.
        Identification of phenyl-substituted acid responsive operons in Ruminococcus albus using differential display RT-PCR.
        in: Proc. 99th Annu. General Mtg. Am. Soc. Microbiol, Washington, DC1999: 1-7

      42. Larson, M. A., and M. Morrison. 1999. Application of the differerential-display RT-PCR technique to examine conditional gene expression in Ruminococcus albus. In Proc. 8th Int. Symp.Microbial Ecol. (in press)

        • Latham M.J.
        Adhesion of rumen bacteria to plant cell walls.
        in: Berkeley R.C.W. Microbial Adhesion to Surfaces. Ellis Horwood, Ltd., Chichester1980: 339-350
        • Latham M.J.
        • Brooker B.E.
        • Petipher G.L.
        • Harris P.J.
        Ruminococcus flavefaciens cell coat and adhesion to cotton cellulose and cell walls in leaves of perennial ryegrass.
        Appl. Environ. Microbiol. 1978; 35: 156-165
        • Latham M.J.
        • Brooker B.E.
        • Petipher G.L.
        • Harris P.J.
        Adhesion of Bacteroides succinogenes in pure cultures and in the presence of Ruminococcus flavefaciens to cell walls in leaves of perennial ryegrass.
        Appl. Environ. Microbiol. 1978; 35: 1166-1173
        • Lindberg F.
        • Lund B.
        • Johansson L.
        • Normark S.
        Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus.
        Nature. 1987; 328: 84-87
        • Malburg L.M.
        • Forsberg C.W.
        Fibrobacter succinogenes possesses at least nine distinct glucanase genes.
        Can. J. Microbiol. 1993; 39: 882-891
        • Malburg S.R.C.
        • Malburg L.M.
        • Liu T.
        • Iyo A.H.
        • Forsberg C.W.
        Catalytic properties of the cellulose-binding endoglucanase F from Fibrobacter succinogenes S85.
        Appl. Environ. Microbiol. 1997; 63: 2449-2453
        • Mcallister T.A.
        • Bae H.D.
        • Jones G.A.
        • Cheng K.J.
        Microbial attachment and feed digestion in the rumen.
        J. Anim. Sci. 1994; 72: 3004-3018
        • Mcgavin M.
        • Forsberg C.W.
        Catalytic and substrate binding domains of endoglucanase 2 from Bacteroides succinogenes.
        J. Bacteriol. 1989; 171: 3310-3315
        • Minato H.
        • Misumori M.
        • Cheng K.J.
        Attachment of microorganisms to solid substrates in the rumen.
        in: Proc. MIE Bioforum on Genetic, Biochemistry and Ecology of Lignocellulose Degradation. Institut Pasteur, Paris, France1993: 139-145
        • Miron J.
        • Ben-Ghedalia D.
        The degradation and utilization of wheat straw cell wall monosaccharide components by defined ruminal cellulolytic bacteria.
        Appl. Microbiol. Biotechnol. 1992; 38: 432-437
        • Miron J.
        • Ben-Ghedalia D.
        Untreated and delignified cotton stalks as model substrates for degradation and utilization of cell wall monosaccharide components by defined ruminal cellulolytic bacteria.
        Bioresource Technol. 1993; 43: 241-247
        • Miron J.
        • Ben-Ghedalia D.
        Digestion of structural poly-saccharides of panicum and vetch hays by the rumen bacterial strains Fibrobacter succinogenes BL2 and Butyrivibrio fibrisolvens D1.
        Appl. Microbiol. Biotechnol. 1993; 39: 756-759
        • Miron J.
        • Ben-ghedalia D.
        Digestion of cell wall monosaccharides of ryegrass and alfalfa hays by the rumen bacteria Fibrobacter succinogenes and Butyrivibrio fibrisolvens.
        Can. J. Microbiol. 1993; 39: 780-786
        • Miron J.
        • Ben-ghedalia D.
        • Yokoyama M.T.
        • Lamed R.
        Some aspects of cellobiose effect on cell surface structures involved in lucerne cell walls utilization by fresh isolates of rumen bacteria.
        Anim. Feed Sci. Technol. 1990; 30: 107-120
        • Miron J.
        • Duncan S.H.
        • Stewart C.S.
        Interactions between rumen bacterial strains during the degradation and utilization of the monosaccharides of barley straw cell walls.
        J. Appl. Bacteriol. 1994; 76: 282-287
        • Miron J.
        • Forsberg C.I.
        Features of Fibrobacter intestinalis DR7 mutant which is impaired with its ability to adhere to cellulose.
        Anaerobe. 1998; 4: 35-43
        • Miron J.
        • Forsberg C.I.
        Characterisation of cellulose binding proteins which are involved in adhesion mechanism of Fibrobacter intestinalis DR7.
        Appl. Microbiol. Biotechnol. 1999; 51: 491-497
        • Miron J.
        • Morag E.
        • Bayer E.A.
        • Lamed R.
        • Ben-ghedalia D.
        An adhesion defective mutant of Ruminococcus albus SY3 is impaired in its capability to degrade cellulose.
        J. Appl. Microbiol. 1998; 84: 249-254
        • Miron J.
        • Yokoyama M.
        • Lamed R.
        Bacterial cell surface structures involved in lucerne cell wall degradation by pure cultures of cellulolytic rumen bacteria.
        Appl. Microbiol. Biotechnol. 1989; 32: 218-222
        • Mitsumori M.
        • Minato H.
        Distribution of cellulose-binding proteins among the representative strains of rumen bacteria.
        J. Gen Appl. Microbiol. 1995; 41: 297-306
        • Mitsumori M.
        • Minato H.
        Cellulose-binding proteins from rumen microorganisms.
        in: Onodera R. Itabashi H. Ushida K. Yano H. Sasaki Y. Rumen Microbes and Digestive Physiology in Ruminants. Japan Scientific Societies Press, Tokyo, Japan1997: 47-57
        • Morris E.J.
        Characteristics of the adhesion of Ruminococcus albus to cellulose.
        FEMS Microbiol. Lett. 1988; 51: 113-118
        • Morris E.J.
        • Cole O.J.
        Relationship between cellulolytic activity and adhesion to cellulose in Ruminococcus albus.
        J Gen. Microbiol. 1987; 133: 1023-1032
        • Morrison M.
        • Miron J.
        Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins?.
        FEMS Microbiol. Letters. 2000; 185: 109-115
        • Mosoni P.
        • Fonty G.
        • Gouet P.
        Competition between ruminal cellulolytic bacteria for adhesion to cellulose.
        Curr. Microbiol. 1997; 35: 44-47
        • Nagamine T.
        • Aminov R.I.
        • Ogata K.
        • Sugiura M.
        • Tajima K.
        • Benno Y.
        Cloning of xylanase genes from Ruminococcus albus and chromosome mapping of Fibrobacter succinogenes.
        in: Onodera R. Itabashi H. Ushida K. Yano H. Sasaki Y. Rumen Microbes and Digestive Physiology in Ruminants. Japan Scientific Societies Press, Tokyo, Japan1997: 59-67
        • Ohara H.
        • Karita S.
        • Kimura T.
        • Sakka K.
        • Ohmiya K.
        Characterization of cellulolytic complex (cellulosome) from Ruminococcus albus.
        Biosci. Biotechnol. Biochem. 2000; 64: 254-260
        • Orpin C.G.
        • Joblin K.N.
        The rumen anaerobic fungi.
        in: Hobson P.N. Stewart C.S. The Rumen Microbial Ecosystem. Blackie Academic and Professonal, Publishers, London.1997: 140-195
        • Patterson H.A.
        • Irvin R.
        • Costerton J.W.
        • Cheng K.J.
        Ultrastructure and adhesion properties of Ruminococcus albus.
        J Bacteriol. 1975; 122: 278-287
        • Pages S.
        • Belaich A.
        • Belaich J.P.
        • Morag E.
        • Lamed R.
        • Shoham Y.
        • Bayer E.A.
        Species-specificity of the cohesin-dockerin interaction between Clostridium thermocellum and Clostridium cellulolyticum: prediction of specificity determinants of the dockerin domain.
        Proteins. 1997; 29: 517-527
        • Pegden R.S.
        • Larson M.A.
        • Grant R.J.
        • Morrison M.
        Adherence of the gram-positive bacterium Ruminococcus albus to cellulose and identification of a novel form of cellulose-binding protein which belongs to the Pil family of proteins.
        J. Bacteriol. 1998; 180: 5921-5927
        • Pell A.N.
        • Schofield P.
        Microbial adhesion and degradation of plant cell walls.
        in: Hatfield R.D. Jung H.G. Ralph J. Buxton D.R. Mertens D.R. Weimer P.J. Forage Cell Wall Structure and Digestibility. ASA-CSSA-SSSA, Madison, WI1993: 397-423
        • Poole D.M.
        • Hazlewood G.P.
        • Laurie J.I.
        • Barker P.J.
        • Gilbert H.J.
        Nucleotide Sequence of the Ruminococcus albus SY3 endoglucanase genes celA and celB.
        Mol. Gen. Genet. 1990; 223: 217-223
        • Rasmussen M.A.
        • White B.A.
        • Hespell R.B.
        Improved assay for quantitating adherence of ruminal bacteria to cellulose.
        Appl. Environ. Microbiol. 1989; 55: 2089-2091
        • Reddy S.K.K.
        • Morrison M.
        Biochemical and molecular characterization of adherence-defective mutants of Ruminococcus albus strain 8.
        Proc. MIE Bioforum on Cellulose Degradation. Institut Pasteur, Paris, France1998 (Page 132)
        • Roger V.
        • Fonty G.
        • Komisarczuk-Bondy S.
        • Gouet P.
        Effects of physiochemical factors on the adhesion to cellulose avicel of the ruminal bacteria Ruminococcus flavefaciens and Fibrobacter succinogenes.
        Appl. Environ Microbiol. 1990; 56: 3081-3087
        • Russell J.B.
        Fermentation of cellodextrins by cellulolytic and non-cellulolytic rumen bacteria.
        Appl. Environ. Microbiol. 1985; 49: 572-576
        • Stack R.J.
        • Hungate R.E.
        Effect of 3-phenylpropanoic acid on capsule and cellulases of Ruminococcus albus 8.
        Appl. Environ. Microbiol. 1984; 48: 218-223
        • Shi Y.
        • Weimer P.J.
        Response surface analysis of the effects of pH and dilution rayte on Ruminococcus flavefaciens FD-1 in cellulose-fed continuous culture.
        Appl. Environ. Microbiol. 1992; 58: 2583-2591
        • Stewart C.S.
        • Duncan S.H.
        • Flint H.J.
        The properties of forms of Ruminococcus flavefaciens which differ in their ability to degrade cotton cellulose.
        FEMS Microbiol. Lett. 1990; 72: 47-50
        • Stewart C.S.
        • Flint H.J.
        • Bryant M.P.
        The rumen bacteria.
        in: Hobson P.N. Stewart C.S. The Rumen Microbial Ecosystem. Blackie Academic and Professional Publishers, London1997: 10-72
        • Tomme P.
        • Warren R.A.J.
        • Gilkes N.R.
        Cellulose hydrolysis by bacteria and fungi.
        Advances in Microbial Physiology. 1995; 37: 1-81
        • Weimer P.J.
        Why don’t ruminal bacteria digest cellulose faster? J.
        Dairy Sci. 1996; 79: 1496-1502
        • Weimer P.J.
        • Schmidt J.K.
        Attachment of Fibrobacter succinogenes to cellulose and cellulose derivatives.
        U.S. Dairy Forage Research Center, 1989 research summaries. USDA, Madison, WI1989 (64–65)
        • Wells J.E.
        • Russell J.B.
        • Shi Y.
        • Weimer P.J.
        Cellodextrin efflux by the cellulolytic ruminal bacterium Fibrobacter succinogenes and its potential role in the growth of nonadherent bacteria.
        Appl. Environ. Microbiol. 1995; 61: 1757-1762
        • White B.A.
        • Cann I.K.O.
        • Mackie R.I.
        • Morrison M.
        Cellulase and xylanase genes from ruminal bacteria: domain analysis suggest a non-cellulosome-like model for organization of the cellulase complex.
        in: Onodera R. Itabashi H. Ushida K. Yano H. Sasaki Y. Rumen Microbes and Digestive Physiology in Ruminants. Japan Scientific Societies Press, Tokyo, Japan1997: 69-80
        • Williams A.G.
        • Coleman G.S.
        The rumen protozoa.
        in: Hobson P.N. Stewart C.S. The Rumen Microbial Ecosystem. Blackie Academic and Professional Publishers, London1997: 73-139
        • Williams A.G.
        • Strachan N.H.
        Polysaccharide degrading enzymes in microbial populations from the liquid and solid fractions of bovine rumen digesta.
        Can. J. Anim. Sci. 1984; 64: 58-59
        • Wood T.M.
        • Wilson C.A.
        • Stewart C.S.
        Preparation of cellulase from the cellulolytic anaerobic rumen bacterium Ruminococcus albus and its release from the bacterial cell wall.
        Biochem. J. 1982; 205: 129-137
        • Yeung M.
        • Cisar J.O.
        Sequence homology between the subunits of two immuno logically and functionally distinct types of fimbriae of Actinomyces spp.
        J Bacteriol. 1990; 172: 2462-2468

      Article info

      Publication history

      Accepted: December 12, 2000
      Received: October 2, 2000

      Identification

      DOI: https://doi.org/10.3168/jds.S0022-0302(01)70159-2

      Copyright

      © 2001 American Dairy Science Association. Published by Elsevier Inc.

      User license

      Elsevier user license |
      How you can reuse Information Icon
      Elsevier user license

      Permitted

      For non-commercial purposes:

      • Read, print & download
      • Text & data mine
      • Translate the article

      Not Permitted

      • Reuse portions or extracts from the article in other works
      • Redistribute or republish the final article
      • Sell or re-use for commercial purposes

      Elsevier's open access license policy

      ScienceDirect

      Access this article on ScienceDirect
      We use cookies to help provide and enhance our service and tailor content. To update your cookie settings, please visit the for this site.
      Copyright © 2023 Elsevier Inc. except certain content provided by third parties. The content on this site is intended for healthcare professionals.


      RELX