Nature’s bioreactor: the rumen as a model for biofuel production

• Lynd LR, Weimer PJ, Van Zyl WH, Pretorius IS. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol. Mol. Biol. Rev.66(3),506–577 (2002).
   PubMed Web of Science ®Google Scholar
• Weimer PJ. Why don’t ruminal bacteria digest cellulose faster? J. Dairy Sci.79(8),1496–1502 (1996).
   PubMed Web of Science ®Google Scholar
• Weimer PJ. End product yields from the extraruminal fermentation of various polysaccharide, protein and nucleic acid components of biofuels feedstocks. Bioresour. Technol.102(3),3254–3259 (2011).
   PubMed Web of Science ®Google Scholar
• Lynd LR, Van Zyl WH, Mcbride JE, Laser M. Consolidated bioprocessing of cellulosic biomass: an update. Curr. Opin. Biotechnol.16(5),577–583 (2005).
   PubMed Web of Science ®Google Scholar
• Weimer PJ, Russell JB, Muck RE. Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. Bioresour. Technol.100(21),5323–5331 (2009).
   PubMed Web of Science ®Google Scholar
• Mackie RI. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr. Comp. Biol.42(2),319–326 (2002).
   PubMed Web of Science ®Google Scholar
• Patra AK, Saxena J. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie Van Leeuwenhoek96(4),363–375 (2009).
   PubMed Web of Science ®Google Scholar
• Fouts DE, Szpakowski S, Purushe J et al. Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS ONE7(11),e48289 (2012).
   PubMed Web of Science ®Google Scholar
• Sauer M, Marx H, Mattanovich D. From rumen to industry. Microb. Cell Fact.11,121 (2012).
   PubMedGoogle Scholar
• Jami E, Mizrahi I. Composition and similarity of bovine rumen microbiota across individual animals. PLoS ONE7(3),e33306 (2012).
   PubMed Web of Science ®Google Scholar
• Bryant MP, Robinson IM. Some nutritional characteristics of predominant culturable ruminal bacteria. J. Bacteriol.84,605–614 (1962).
   PubMed Web of Science ®Google Scholar
• Bryant MP, Burkey LA. Cultural methods and some characteristics of some of the more numerous groups of bacteria in the bovine rumen. J. Dairy Sci.36,205–217 (1953).
   Web of Science ®Google Scholar
• Varel VH, Dehority BA. Ruminal cellulolytic bacteria and protozoa from bison, cattle–bison hybrids, and cattle fed three alfalfa-corn diets. Appl. Environ. Microbiol.55(1),148–153 (1989).
   PubMed Web of Science ®Google Scholar
• Stevenson DM, Weimer PJ. Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl. Microbiol. Biotechnol.75(1),165–174 (2007).
   PubMed Web of Science ®Google Scholar
• Kim M, Morrison M, Yu Z. Phylogenetic diversity of bacterial communities in bovine rumen as affected by diets and microenvironments. Folia Microbiol. (Praha)56(5),453–458 (2011).
   PubMed Web of Science ®Google Scholar
• Hess M, Sczyrba A, Egan R et al. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science331(6016),463–467 (2011).
   PubMed Web of Science ®Google Scholar
• Hungate RE. The anaerobic mesophilic cellulolytic bacteria. Bacteriol. Rev.14(1),1–49 (1950).
   PubMedGoogle Scholar
• Dehority BA, Tirabasso PA. Antibiosis between ruminal bacteria and ruminal fungi. Appl. Environ. Microbiol.66(7),2921–2927 (2000).
   PubMed Web of Science ®Google Scholar
• Wood TM, Wilson CA, Mccrae SI, Joblin KN. A highly-active extracellular cellulase from the anaerobic rumen fungus Neocallimastix-frontalis.FEMS Microbiol. Lett.34(1),37–40 (1986).
   Web of Science ®Google Scholar
• Youssef NH, Couger M, Struchtemeyer CG et al. The genome of the anaerobic fungus Orpinomyces sp. C1A reveals the unique evolutionary history of a remarkable plant biomass degrader. Appl. Environ. Microbiol.79(15),4620–4634 (2013).
   PubMed Web of Science ®Google Scholar
• Ransom-Jones E, Jones DL, Mccarthy AJ, Mcdonald JE. The Fibrobacteres: an important phylum of cellulose-degrading bacteria. Microb. Ecol.63(2),267–281 (2012).
   PubMed Web of Science ®Google Scholar
• Weimer PJ. Effects of dilution rate and pH on the ruminal cellulolytic bacterium Fibrobacter succinogenes S85 in cellulose-fed continuous culture. Arch. Microbiol.160(4),288–294 (1993).
   PubMed Web of Science ®Google Scholar
• Suen G, Weimer PJ, Stevenson DM et al. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE6(4),e18814 (2011).
   PubMed Web of Science ®Google Scholar
• Jun HS, Qi M, Gong J, Egbosimba EE, Forsberg CW. Outer membrane proteins of Fibrobacter succinogenes with potential roles in adhesion to cellulose and in cellulose digestion. J. Bacteriol.189(19),6806–6815 (2007).
   PubMed Web of Science ®Google Scholar
• Pavlostathis SG, Miller TL, Wolin MJ. Fermentation of insoluble cellulose by continuous cultures of Ruminococcus albus.Appl. Environ. Microbiol.54(11),2655–2659 (1988).
   PubMed Web of Science ®Google Scholar
• Weimer PJ, Price NP, Kroukamp O, Joubert LM, Wolfaardt GM, Van Zyl WH. Studies of the extracellular glycocalyx of the anaerobic cellulolytic bacterium Ruminococcus albus 7. Appl. Environ. Microbiol.72(12),7559–7566 (2006).
   PubMed Web of Science ®Google Scholar
• Miron J, Jacobovitch J, Bayer EA, Lamed R, Morrison M, Ben-Ghedalia D. Subcellular distribution of glycanases and related components in Ruminococcus albus SY3 and their role in cell adhesion to cellulose. J. Appl. Microbiol.91(4),677–685 (2001).
   PubMed Web of Science ®Google Scholar
• Ohara H, Karita S, Kimura T, Sakka K, Ohmiya K. Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus.Biosci. Biotechnol. Biochem.64(2),254–260 (2000).
   PubMed Web of Science ®Google Scholar
• Suen G, Stevenson DM, Bruce DC et al. Complete genome of the cellulolytic ruminal bacterium Ruminococcus albus 7. J. Bacteriol.193(19),5574–5575 (2011).
   PubMed Web of Science ®Google Scholar
• Moon YH, Iakiviak M, Bauer S, Mackie RI, Cann IK. Biochemical analyses of multiple endoxylanases from the rumen bacterium Ruminococcus albus 8 and their synergistic activities with accessory hemicellulose-degrading enzymes. Appl. Environ. Microbiol.77(15),5157–5169 (2011).
   PubMed Web of Science ®Google Scholar
• Morrison M, Miron J. Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? FEMS Microbiol. Lett.185(2),109–115 (2000).
   PubMed Web of Science ®Google Scholar
• Berg Miller ME, Antonopoulos DA, Rincon MT et al. Diversity and strain specificity of plant cell wall degrading enzymes revealed by the draft genome of Ruminococcus flavefaciens FD-1. PLoS ONE4(8),e6650 (2009).
   PubMedGoogle Scholar
• Rincon MT, Dassa B, Flint HJ et al. Abundance and diversity of dockerin-containing proteins in the fiber-degrading rumen bacterium, Ruminococcus flavefaciens FD-1. PLoS ONE5(8),e12476 (2010).
   PubMedGoogle Scholar
• Purushe J, Fouts DE, Morrison M et al. Comparative genome analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microb. Ecol.60(4),721–729 (2010).
   PubMed Web of Science ®Google Scholar
• Kelly WJ, Leahy SC, Altermann E et al. The glycobiome of the rumen bacterium Butyrivibrio proteoclasticus B316(T) highlights adaptation to a polysaccharide-rich environment. PLoS ONE5(8),e11942 (2010).
   PubMed Web of Science ®Google Scholar
• Iakiviak M, Mackie RI, Cann IK. Functional analyses of multiple lichenin-degrading enzymes from the rumen bacterium Ruminococcus albus 8. Appl. Environ. Microbiol.77(21),7541–7550 (2011).
   PubMed Web of Science ®Google Scholar
• Flint HJ, Martin J, Mcpherson CA, Daniel AS, Zhang JX. A bifunctional enzyme, with separate xylanase and beta(1,3–1,4)-glucanase domains, encoded by the xynD gene of Ruminococcus flavefaciens.J. Bacteriol.175(10),2943–2951 (1993).
   PubMed Web of Science ®Google Scholar
• Nakamura M, Nagamine T, Harada C, Tajima K, Matsui H, Benno Y. Expression of Ruminococcus albus xylanase gene (xynA) in Streptococcus bovis 12-U-1. Curr. Microbiol.47(1),71–74 (2003).
   PubMed Web of Science ®Google Scholar
• Ljungdahl LG. The cellulase/hemicellulase system of the anaerobic fungus Orpinomyces PC-2 and aspects of its applied use. Ann. NY Acad. Sci.1125,308–321 (2008).
   PubMed Web of Science ®Google Scholar
• Liu JR, Duan CH, Zhao X, Tzen JT, Cheng KJ, Pai CK. Cloning of a rumen fungal xylanase gene and purification of the recombinant enzyme via artificial oil bodies. Appl. Microbiol. Biotechnol.79(2),225–233 (2008).
   PubMed Web of Science ®Google Scholar
• Yang B, Dai Z, Ding S, Wyman CE. Enzymatic hydrolysis of cellulosic biomass. Biofuels2,421–450 (2011).
   Google Scholar
• Himmel M, Xu Q, Luo Y, Ding S, Lamed R, Bayer EA. Microbial enzyme systems for biomass conversion: emerging paradigms. Biofuels1,323–341 (2010).
   Google Scholar
• Osborne JM, Dehority BA. Synergism in degradation and utilization of intact forage cellulose, hemicellulose, and pectin by three pure cultures of ruminal bacteria. Appl. Environ. Microbiol.55(9),2247–2250 (1989).
   PubMed Web of Science ®Google Scholar
• Fukuma N, Koike S, Kobayashi Y. Involvement of recently cultured group U2 bacterium in ruminal fiber digestion revealed by coculture with Fibrobacter succinogenes S85. FEMS Microbiol. Lett.336(1),17–25 (2012).
   PubMed Web of Science ®Google Scholar
• Fondevila M, Dehority BA. Interactions between Fibrobacter succinogenes, Prevotella ruminicola, and Ruminococcus flavefaciens in the digestion of cellulose from forages. J. Anim. Sci.74(3),678–684 (1996).
   PubMed Web of Science ®Google Scholar
• Russell JB, Mantovani HC. The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J. Mol. Microbiol. Biotechnol.4(4),347–355 (2002).
   PubMed Web of Science ®Google Scholar
• Kisidayova S, Laukova A, Jalc D. Comparison of nisin and monensin effects on ciliate and selected bacterial populations in artificial rumen. Folia Microbiol. (Praha)54(6),527–532 (2009).
   PubMed Web of Science ®Google Scholar
• Callaway TR, Carneiro De Melo AM, Russell JB. The effect of nisin and monensin on ruminal fermentations in vitro. Curr. Microbiol.35(2),90–96 (1997).
   PubMed Web of Science ®Google Scholar
• Chen J, Stevenson DM, Weimer PJ. Albusin B, a bacteriocin from the ruminal bacterium Ruminococcus albus 7 that inhibits growth of Ruminococcus flavefaciens.Appl. Environ. Microbiol.70(5),3167–3170 (2004).
   PubMed Web of Science ®Google Scholar
• Steinkraus KH. Industrialization of Indigenous Fermented Foods (Second Edition). Marcel Dekker, NY, USA (2004).
   Google Scholar
• Warnecke F, Luginbuhl P, Ivanova N et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature450(7169),560–565 (2007).
   PubMed Web of Science ®Google Scholar
• Breznak J, Brune A. Role of microorganisms in the digestion of lignocelluloses by termintes. Annu. Rev. Microbiol.39,453–487 (1994).
   Google Scholar
• Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, Scharf ME. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes.Biotechnol. Biofuels2,25 (2009).
   PubMedGoogle Scholar
• Luyten YA, Thompson JR, Morrill W, Polz MF, Distel DL. Extensive variation in intracellular symbiont community composition among members of a single population of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl. Environ. Microbiol.72(1),412–417 (2006).
   PubMed Web of Science ®Google Scholar
• Yang JC, Madupu R, Durkin AS et al. The complete genome of Teredinibacter turnerae T7901: an intracellular endosymbiont of marine wood-boring bivalves (shipworms). PLoS ONE4(7),e6085 (2009).
   PubMed Web of Science ®Google Scholar
• Imam SH, Greene RV, Griffin HL. Binding of extracellular carboxymethylcellulase activity from the marine shipworm bacterium to insoluble cellulosic substrates. Appl. Environ. Microbiol.59(5),1259–1263 (1993).
   PubMed Web of Science ®Google Scholar
• Greene RV, Griffin HL, Freer SN. Purification and characterization of an extracellular endoglucanase from the marine shipworm bacterium. Arch. Biochem. Biophys.267(1),334–341 (1988).
   PubMed Web of Science ®Google Scholar
• Ekborg NA, Morrill W, Burgoyne AM, Li L, Distel DL. CelAB, a multifunctional cellulase encoded by Teredinibacter turnerae T7902T, a culturable symbiont isolated from the wood-boring marine bivalve Lyrodus pedicellatus.Appl. Environ. Microbiol.73(23),7785–7788 (2007).
   PubMed Web of Science ®Google Scholar
• Ni J, Takehara M, Watanabe H. Heterologous overexpression of a mutant termite cellulase gene in Escherichia coli by DNA shuffling of four orthologous parental cDNAs. Biosci. Biotechnol. Biochem.69(9),1711–1720 (2005).
   PubMed Web of Science ®Google Scholar
• Nimchua T, Thongaram T, Uengwetwanit T, Pongpattanakitshote S, Eurwilaichitr L. Metagenomic analysis of novel lignocellulose-degrading enzymes from higher termite guts inhabiting microbes. J. Microbiol. Biotechnol.22(4),462–469 (2012).
   PubMed Web of Science ®Google Scholar
• Brulc JM, Antonopoulos DA, Miller ME et al. Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc. Natl Acad. Sci. USA106(6),1948–1953 (2009).
   PubMed Web of Science ®Google Scholar
• Mckinlay JB, Laivenieks M, Schindler BD et al. A genomic perspective on the potential of Actinobacillus succinogenes for industrial succinate production. BMC Genomics11,680 (2010).
   PubMed Web of Science ®Google Scholar
• Spring S, Lapidus A, Schroder M et al. Complete genome sequence of Desulfotomaculum acetoxidans type strain (5575). Stand. Genomic Sci.1(3),242–253 (2009).
   PubMed Web of Science ®Google Scholar
• Roh H, Ko HJ, Kim D et al. Complete genome sequence of a carbon monoxide-utilizing acetogen, Eubacterium limosum KIST612. J. Bacteriol.193(1),307–308 (2011).
   PubMed Web of Science ®Google Scholar
• Forde BM, Neville BA, O’Donnell MM et al. Genome sequences and comparative genomics of two Lactobacillus ruminis strains from the bovine and human intestinal tracts. Microb. Cell Fact.10(Suppl. 1),S13 (2011).
   PubMedGoogle Scholar
• Hong SH, Kim JS, Lee SY et al. The genome sequence of the capnophilic rumen bacterium Mannheimia succiniciproducens.Nat. Biotechnol.22(10),1275–1281 (2004).
   PubMed Web of Science ®Google Scholar
• Marx H, Graf AB, Tatto NE, Thallinger GG, Mattanovich D, Sauer M. Genome sequence of the ruminal bacterium Megasphaera elsdenii.J. Bacteriol.193(19),5578–5579 (2011).
   PubMed Web of Science ®Google Scholar
• Lee GH, Kumar S, Lee JH et al. Genome sequence of Oscillibacter ruminantium strain GH1, isolated from rumen of Korean native cattle. J. Bacteriol.194(22),6362 (2012).
   PubMed Web of Science ®Google Scholar
• Berg Miller ME, Yeoman CJ, Chia N et al. Phage–bacteria relationships and CRISPR elements revealed by a metagenomic survey of the rumen microbiome. Environ. Microbiol.14(1),207–227 (2012).
   PubMed Web of Science ®Google Scholar
• Pukall R, Lapidus A, Nolan M et al. Complete genome sequence of Slackia heliotrinireducens type strain (RHS 1). Stand. Genomic Sci.1(3),234–241 (2009).
   PubMed Web of Science ®Google Scholar
• Rusniok C, Couve E, Da Cunha V et al. Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J. Bacteriol.192(8),2266–2276 (2010).
   PubMed Web of Science ®Google Scholar
• Rosewarne CP, Cheung JL, Smith WJ et al. Draft genome sequence of Treponema sp. strain JC4, a novel spirochete isolated from the bovine rumen. J. Bacteriol.194(15),4130 (2012).
   PubMed Web of Science ®Google Scholar
• Baar C, Eppinger M, Raddatz G et al. Complete genome sequence and analysis of Wolinella succinogenes.Proc. Natl Acad. Sci. USA100(20),11690–11695 (2003).
   PubMed Web of Science ®Google Scholar
• Leahy SC, Kelly WJ, Altermann E et al. The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS ONE5(1),e8926 (2010).
   PubMedGoogle Scholar
• Lee JH, Rhee MS, Kumar S et al. Genome sequence of Methanobrevibacter sp. strain jh1, isolated from rumen of Korean native cattle. Genome Announc.1(1), pii: e00002-13 (2013).
   Google Scholar

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• Hungate1000 Microbial Genome Projects. www.hungate1000.org.nz/genomes.html
   Google Scholar