Ecology and characteristics of methanogenic archaea in animals and humans

Abstract In this review, the molecular techniques used in animal-based-methanogen studies will be discussed along with how methanogens interact not only with other microorganisms but with their animal hosts as well. These methods not only indicate the diversity and levels of methanogens, but also provide insight on their ecological functions. Most molecular techniques have been based on either 16S rRNA genes or methyl-coenzyme M reductase, a ubiquitous enzyme in methanogens. The most predominant methanogens in animals belong to the genus Methanobrevibacter. Besides methanogens contributing to overall H2 balance, methanogens also have mutual interactions with other bacteria. In addition to shared metabolic synergism, the host animal retrieves additional energy from the diet when methanogens are co-colonized with other normal flora. By comparing genes in methanogens with other bacteria, possible gene transfer between methanogens and other bacteria in the same environments appears to occur. Finally, diets in conjunction with the genetics of methanogens and hosts may represent the biological framework that dictate the extent of methanogen prevalence in these ecosystems. In addition, host evolution including the immune system could serve as an additional selective pressure for methanogen colonization.

[1]  J. Reinus,et al.  Gastrointestinal anatomy and physiology , 2016 .

[2]  W. Doolittle,et al.  Archaea , 2015, Current Biology.

[3]  R. E. Hungate,et al.  The Rumen and Its Microbes , 2013 .

[4]  A. Brune,et al.  “Methanoplasmatales,” Thermoplasmatales-Related Archaea in Termite Guts and Other Environments, Are the Seventh Order of Methanogens , 2012, Applied and Environmental Microbiology.

[5]  B. Dridi,et al.  Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. , 2012, International journal of systematic and evolutionary microbiology.

[6]  K. Beauchemin,et al.  Structures of free-living and protozoa-associated methanogen communities in the bovine rumen differ according to comparative analysis of 16S rRNA and mcrA genes. , 2012, Microbiology.

[7]  A. Wright,et al.  Molecular Diversity of Methanogens in Fecal Samples From Captive Sumatran Orangutans (Pongo abelii) , 2012, American journal of primatology.

[8]  L. Barton,et al.  Microbe–Microbe Interactions , 2011 .

[9]  L. Shek,et al.  Evaluation of stool microbiota signatures in two cohorts of Asian (Singapore and Indonesia) newborns at risk of atopy , 2011, BMC Microbiology.

[10]  D. Raoult,et al.  Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii , 2011, International Journal of Obesity.

[11]  R. Oozeer,et al.  Transmission of Intestinal Bifidobacterium longum subsp. longum Strains from Mother to Infant, Determined by Multilocus Sequencing Typing and Amplified Fragment Length Polymorphism , 2011, Applied and Environmental Microbiology.

[12]  H. Gaskins,et al.  Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon , 2011, The ISME Journal.

[13]  A. Wright,et al.  Differences in the Rumen Methanogen Populations of Lactating Jersey and Holstein Dairy Cows under the Same Diet Regimen , 2011, Applied and Environmental Microbiology.

[14]  J. Neu,et al.  Cesarean versus vaginal delivery: long-term infant outcomes and the hygiene hypothesis. , 2011, Clinics in perinatology.

[15]  M. Steele,et al.  Impact of High-Concentrate Feeding and Low Ruminal pH on Methanogens and Protozoa in the Rumen of Dairy Cows , 2011, Microbial Ecology.

[16]  P. Janssen,et al.  Methanogen community structure in the rumens of farmed sheep, cattle and red deer fed different diets. , 2011, FEMS microbiology ecology.

[17]  J. Neu,et al.  The developing intestinal microbiome and its relationship to health and disease in the neonate , 2011, Journal of Perinatology.

[18]  Jesse R. Zaneveld,et al.  Pan-genome of the dominant human gut-associated archaeon, Methanobrevibacter smithii, studied in twins , 2011, Proceedings of the National Academy of Sciences.

[19]  Weiyun Zhu,et al.  Phylogenetic Analysis of Methanogens in the Pig Feces , 2011, Current Microbiology.

[20]  H. Horz,et al.  The Discussion Goes on: What Is the Role of Euryarchaeota in Humans? , 2010, Archaea.

[21]  G. Avguštin,et al.  Molecular profiling and identification of methanogenic archaeal species from rabbit caecum. , 2010, FEMS microbiology ecology.

[22]  R. Forster,et al.  Quantitative Fluorescence In Situ Hybridization of Microbial Communities in the Rumens of Cattle Fed Different Diets , 2010, Applied and Environmental Microbiology.

[23]  L. T. Angenent,et al.  Succession of microbial consortia in the developing infant gut microbiome , 2010, Proceedings of the National Academy of Sciences.

[24]  K. Nielsen,et al.  Ecological Characterisation of the Colonic Microbiota in Arctic and Sub-Arctic Seals , 2010, Microbial Ecology.

[25]  A. Gasbarrini,et al.  The Role of Methane in Intestinal Diseases , 2010, The American Journal of Gastroenterology.

[26]  J. Doré,et al.  Molecular evaluation of the human gut methanogenic archaeal microbiota reveals an age-associated increase of the diversity. , 2010, Environmental microbiology reports.

[27]  S. Takashiba,et al.  Antigenic group II chaperonin in Methanobrevibacter oralis may cross-react with human chaperonin CCT. , 2010, Molecular oral microbiology.

[28]  A. Schwiertz,et al.  Microbiota and SCFA in Lean and Overweight Healthy Subjects , 2010, Obesity.

[29]  S. Ricke,et al.  Dilution rates influence ammonia‐assimilating enzyme activities and cell parameters of Selenomonas ruminantium strain D in continuous (glucose‐limited) culture , 2010, Journal of applied microbiology.

[30]  P. Weimer,et al.  Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. , 2009, Bioresource technology.

[31]  A. Wright,et al.  Rumen-like methanogens identified from the crop of the folivorous South American bird, the hoatzin (Opisthocomus hoazin) , 2009, The ISME Journal.

[32]  Rob Knight,et al.  Identifying genetic determinants needed to establish a human gut symbiont in its habitat. , 2009, Cell host & microbe.

[33]  Didier Raoult,et al.  High Prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae Detected in the Human Gut Using an Improved DNA Detection Protocol , 2009, PloS one.

[34]  L. Guan,et al.  Assessment of the Microbial Ecology of Ruminal Methanogens in Cattle with Different Feed Efficiencies , 2009, Applied and Environmental Microbiology.

[35]  P. Chaudhary,et al.  Dominance of Methanomicrobium phylotype in methanogen population present in Murrah buffaloes (Bubalus bubalis) , 2009, Letters in applied microbiology.

[36]  H. Matsumoto,et al.  Influence of Maternal Bifidobacteria on the Establishment of Bifidobacteria Colonizing the Gut in Infants , 2009, Pediatric Research.

[37]  J. Regan,et al.  mcrA-Targeted Real-Time Quantitative PCR Method To Examine Methanogen Communities , 2009, Applied and Environmental Microbiology.

[38]  M. Crowell,et al.  Human gut microbiota in obesity and after gastric bypass , 2009, Proceedings of the National Academy of Sciences.

[39]  P. Evans,et al.  Community Composition and Density of Methanogens in the Foregut of the Tammar Wallaby (Macropus eugenii) , 2009, Applied and Environmental Microbiology.

[40]  P. Weimer,et al.  Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen. , 2009, FEMS microbiology ecology.

[41]  J. Edwards,et al.  Molecular Diversity of the Rumen Microbiome of Norwegian Reindeer on Natural Summer Pasture , 2009, Microbial Ecology.

[42]  S. Ragsdale,et al.  Acetogenesis and the Wood-Ljungdahl pathway of CO(2) fixation. , 2008, Biochimica et biophysica acta.

[43]  R. Knight,et al.  Worlds within worlds: evolution of the vertebrate gut microbiota , 2008, Nature Reviews Microbiology.

[44]  S. Takashiba,et al.  Distribution of Archaea in Japanese patients with periodontitis and humoral immune response to the components. , 2008, FEMS microbiology letters.

[45]  Colin Hill,et al.  Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome , 2008, Proceedings of the National Academy of Sciences.

[46]  A. Munn,et al.  Modelling digestive constraints in non-ruminant and ruminant foregut-fermenting mammals. , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[47]  M. Alric,et al.  A putative new order of methanogenic Archaea inhabiting the human gut, as revealed by molecular analyses of the mcrA gene. , 2008, Research in microbiology.

[48]  Florent E. Angly,et al.  Comparative Metagenomics Reveals Host Specific Metavirulomes and Horizontal Gene Transfer Elements in the Chicken Cecum Microbiome , 2008, PloS one.

[49]  Humberto Ortiz-Zuazaga,et al.  Bacterial Community in the Crop of the Hoatzin, a Neotropical Folivorous Flying Bird , 2008, Applied and Environmental Microbiology.

[50]  A. Wright,et al.  Methanobrevibacter Phylotypes are the Dominant Methanogens in Sheep from Venezuela , 2008, Microbial Ecology.

[51]  Jörg Meyer,et al.  Volatilisation of metals and metalloids: an inherent feature of methanoarchaea? , 2008, Systematic and applied microbiology.

[52]  M. Hamady,et al.  Evolution of Mammals and Their Gut Microbes , 2008, Science.

[53]  Peter H. Janssen,et al.  Structure of the Archaeal Community of the Rumen , 2008, Applied and Environmental Microbiology.

[54]  Y. Kamagata,et al.  Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov. , 2008, International journal of systematic and evolutionary microbiology.

[55]  H. Horz,et al.  Quantitative Analysis of Three Hydrogenotrophic Microbial Groups, Methanogenic Archaea, Sulfate-Reducing Bacteria, and Acetogenic Bacteria, within Plaque Biofilms Associated with Human Periodontal Disease , 2008, Journal of bacteriology.

[56]  S. Ricke,et al.  Limiting Avian Gastrointestinal Tract Salmonella Colonization by Cecal Anaerobic Bacteria, and a Potential Role for Methanogens , 2008 .

[57]  S. Ricke,et al.  Detection of methane and quantification of methanogenic archaea in faeces from young broiler chickens using real‐time PCR , 2007, Letters in applied microbiology.

[58]  S. Denman,et al.  Quantitation and diversity analysis of ruminal methanogenic populations in response to the antimethanogenic compound bromochloromethane. , 2007, FEMS microbiology ecology.

[59]  J. Gogarten,et al.  Evolution of Acetoclastic Methanogenesis in Methanosarcina via Horizontal Gene Transfer from Cellulolytic Clostridia , 2007, Journal of bacteriology.

[60]  S. Salminen,et al.  Mode of Delivery – Effects on Gut Microbiota and Humoral Immunity , 2007, Neonatology.

[61]  S. Ricke,et al.  Molting in Salmonella Enteritidis-challenged laying hens fed alfalfa crumbles. II. Fermentation and microbial ecology response. , 2007, Poultry science.

[62]  Birgitte Stuer-Lauridsen,et al.  Adaptation and Response of Bifidobacterium animalis subsp. lactis to Bile: a Proteomic and Physiological Approach , 2007, Applied and Environmental Microbiology.

[63]  Daniel B. DiGiulio,et al.  Development of the Human Infant Intestinal Microbiota , 2007, PLoS biology.

[64]  Shiao Y Wang,et al.  Development of a Swine-Specific Fecal Pollution Marker Based on Host Differences in Methanogen mcrA Genes , 2007, Applied and Environmental Microbiology.

[65]  R. Wilson,et al.  Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut , 2007, Proceedings of the National Academy of Sciences.

[66]  S. Turroni,et al.  Binding of Human Plasminogen to Bifidobacterium , 2007, Journal of bacteriology.

[67]  D. Lynn,et al.  Molecular Diversity of Methanogens in Feedlot Cattle from Ontario and Prince Edward Island, Canada , 2007, Applied and Environmental Microbiology.

[68]  S. Ricke,et al.  Comparison of in vitro fermentation and molecular microbial profiles of high-fiber feed substrates incubated with chicken cecal inocula. , 2007, Poultry science.

[69]  J. Hackstein,et al.  The competitive success of Methanomicrococcus blatticola, a dominant methylotrophic methanogen in the cockroach hindgut, is supported by high substrate affinities and favorable thermodynamics. , 2007, FEMS microbiology ecology.

[70]  P. Evans,et al.  Analysis of Methanogen Diversity in the Rumen Using Temporal Temperature Gradient Gel Electrophoresis: Identification of Uncultured Methanogens , 2007, Microbial Ecology.

[71]  J. Bowman,et al.  Methanobrevibacter millerae sp. nov. and Methanobrevibacter olleyae sp. nov., methanogens from the ovine and bovine rumen that can utilize formate for growth. , 2007, International journal of systematic and evolutionary microbiology.

[72]  Christian Vogl,et al.  The bile/arsenite/riboflavin transporter (BART) superfamily , 2007, The FEBS journal.

[73]  E. Mardis,et al.  An obesity-associated gut microbiome with increased capacity for energy harvest , 2006, Nature.

[74]  Zhongtang Yu,et al.  Application of Recent DNA/RNA-based Techniques in Rumen Ecology , 2006 .

[75]  S. Ricke,et al.  Identification and Quantification of Methanogenic Archaea in Adult Chicken Ceca , 2006, Applied and Environmental Microbiology.

[76]  Jeffrey I. Gordon,et al.  Reciprocal Gut Microbiota Transplants from Zebrafish and Mice to Germ-free Recipients Reveal Host Habitat Selection , 2006, Cell.

[77]  H. Harada,et al.  Visualization of mcr mRNA in a methanogen by fluorescence in situ hybridization with an oligonucleotide probe and two-pass tyramide signal amplification (two-pass TSA-FISH). , 2006, Journal of microbiological methods.

[78]  Y. Kamagata,et al.  Application of Pseudomurein Endoisopeptidase to Fluorescence In Situ Hybridization of Methanogens within the Family Methanobacteriaceae , 2006, Applied and Environmental Microbiology.

[79]  J. Gordon,et al.  A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[80]  M. Pop,et al.  Metagenomic Analysis of the Human Distal Gut Microbiome , 2006, Science.

[81]  A. Wright,et al.  Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. , 2006, Anaerobe.

[82]  S. Ricke,et al.  Effects of nitro compounds and feedstuffs on in vitro methane production in chicken cecal contents and rumen fluid. , 2006, Anaerobe.

[83]  H. Horz,et al.  Identification and Quantification of Archaea Involved in Primary Endodontic Infections , 2006, Journal of Clinical Microbiology.

[84]  L. Skillman,et al.  16S rDNA directed PCR primers and detection of methanogens in the bovine rumen , 2006, Letters in applied microbiology.

[85]  Dae-Joong Kang,et al.  Bile salt biotransformations by human intestinal bacteria Published, JLR Papers in Press, November 18, 2005. , 2006, Journal of Lipid Research.

[86]  W. F. Fricke,et al.  The Genome Sequence of Methanosphaera stadtmanae Reveals Why This Human Intestinal Archaeon Is Restricted to Methanol and H2 for Methane Formation and ATP Synthesis , 2006, Journal of bacteriology.

[87]  R. Pearson,et al.  A comparison of the effect of forage type and level of feeding on the digestibility and gastrointestinal mean retention time of dry forages given to cattle, sheep, ponies and donkeys , 2006, British Journal of Nutrition.

[88]  Seigo Shima,et al.  Methyl-coenzyme M reductase and the anaerobic oxidation of methane in methanotrophic Archaea. , 2005, Current opinion in microbiology.

[89]  C. Delbès,et al.  Recovery of Partial 16S rDNA Sequences Suggests the Presence of Crenarchaeota in the Human Digestive Ecosystem , 2005, Current Microbiology.

[90]  C. Hill,et al.  The interaction between bacteria and bile. , 2005, FEMS microbiology reviews.

[91]  J. Apajalahti Comparative Gut Microflora, Metabolic Challenges, and Potential Opportunities , 2005 .

[92]  E. Purdom,et al.  Diversity of the Human Intestinal Microbial Flora , 2005, Science.

[93]  S. Ricke,et al.  Reduction of Salmonella enterica serovar enteritidis colonization and invasion by an alfalfa diet during molt in Leghorn hens. , 2005, Poultry science.

[94]  S. S. Lee,et al.  Phylogenetic analysis of archaea in three fractions of cow rumen based on the 16S rDNA sequence. , 2004, Anaerobe.

[95]  S. Ricke,et al.  Feeding low calcium and zinc molt diets sustains gastrointestinal fermentation and limits Salmonella enterica serovar Enteritidis colonization in laying hens , 2004 .

[96]  P. Evans,et al.  16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. , 2004, Anaerobe.

[97]  M. Mitsumori,et al.  Phylogenetic analysis of methyl coenzyme‐M reductase detected from the bovine rumen , 2004, Letters in applied microbiology.

[98]  A. Margolles,et al.  Effect of the adaptation to high bile salts concentrations on glycosidic activity, survival at low PH and cross-resistance to bile salts in Bifidobacterium. , 2004, International journal of food microbiology.

[99]  B. Wren,et al.  The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. , 2004, Microbiology.

[100]  S. Acinas,et al.  Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons , 2004, Journal of bacteriology.

[101]  D. Relman,et al.  Methanogenic Archaea and human periodontal disease. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[102]  D. Józefiak,et al.  Carbohydrate fermentation in the avian ceca: a review , 2004 .

[103]  C. Christophersen,et al.  Molecular Diversity of Rumen Methanogens from Sheep in Western Australia , 2004, Applied and Environmental Microbiology.

[104]  M. Friedrich,et al.  Microbial Community Structure in Midgut and Hindgut of the Humus-Feeding Larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) , 2003, Applied and Environmental Microbiology.

[105]  A. Wright,et al.  Improved strategy for presumptive identification of methanogens using 16S riboprinting. , 2003, Journal of microbiological methods.

[106]  U. Stingl,et al.  Physicochemical Conditions and Microbial Activities in the Highly Alkaline Gut of the Humus-Feeding Larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) , 2003, Applied and Environmental Microbiology.

[107]  A. Bernalier-Donadille,et al.  The cellulolytic microflora of the human colon: evidence of microcrystalline cellulose-degrading bacteria in methane-excreting subjects. , 2003, FEMS microbiology ecology.

[108]  E. Delong,et al.  Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea , 2003, Applied and Environmental Microbiology.

[109]  R. Joerger,et al.  Composition of microbiota in content and mucus from cecae of broiler chickens as measured by fluorescent in situ hybridization with group-specific, 16S rRNA-targeted oligonucleotide probes. , 2003, Poultry science.

[110]  S. Ricke,et al.  Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. , 2003, Poultry science.

[111]  T. Lueders,et al.  Evaluation of PCR Amplification Bias by Terminal Restriction Fragment Length Polymorphism Analysis of Small-Subunit rRNA and mcrA Genes by Using Defined Template Mixtures of Methanogenic Pure Cultures and Soil DNA Extracts , 2003, Applied and Environmental Microbiology.

[112]  T. Oshima,et al.  Phylogenetic Analysis of Symbiotic Archaea Living in the Gut of Xylophagous Cockroaches , 2002 .

[113]  P. Luton,et al.  The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. , 2002, Microbiology.

[114]  T. Miller,et al.  Description of Methanobrevibacter gottschalkii sp. nov., Methanobrevibacter thaueri sp. nov., Methanobrevibacter woesei sp. nov. and Methanobrevibacter wolinii sp. nov.. , 2002, International journal of systematic and evolutionary microbiology.

[115]  R. Mackie Mutualistic Fermentative Digestion in the Gastrointestinal Tract: Diversity and Evolution1 , 2002, Integrative and comparative biology.

[116]  W. Holben,et al.  Percent G+C Profiling Accurately Reveals Diet-Related Differences in the Gastrointestinal Microbial Community of Broiler Chickens , 2001, Applied and Environmental Microbiology.

[117]  A. Nozhevnikova,et al.  Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature , 2001 .

[118]  T. Lueders,et al.  Axial Differences in Community Structure ofCrenarchaeota and Euryarchaeota in the Highly Compartmentalized Gut of the Soil-Feeding TermiteCubitermes orthognathus , 2001, Applied and Environmental Microbiology.

[119]  R. Aminov,et al.  Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens. , 2001, FEMS microbiology letters.

[120]  R. Forster,et al.  Phylogenetic analysis of methanogens from the bovine rumen , 2001, BMC Microbiology.

[121]  K. Hinni,et al.  Identification of archaeal rDNA from subgingival dental plaque by PCR amplification and sequence analysis. , 2001, FEMS microbiology letters.

[122]  R. Conrad,et al.  Molecular analyses of methyl-coenzyme M reductase alpha-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. , 2001, Environmental microbiology.

[123]  P. Cronje,et al.  Ruminant Physiology: Digestion, Metabolism, Growth and Reproduction , 2000 .

[124]  J. Hackstein,et al.  Methanomicrococcus blatticola gen. nov., sp. nov., a methanol- and methylamine-reducing methanogen from the hindgut of the cockroach Periplaneta americana. , 2000, International journal of systematic and evolutionary microbiology.

[125]  N. Martin,et al.  Shared and unique environmental factors determine the ecology of methanogens in humans and rats , 2000, American Journal of Gastroenterology.

[126]  F. Schneider,et al.  Isolation and characterization of a Lactobacillus amylovorus mutant depleted in conjugated bile salt hydrolase activity: relation between activity and bile salt resistance , 2000, Journal of applied microbiology.

[127]  B. Patel,et al.  Taxonomic, phylogenetic, and ecological diversity of methanogenic Archaea. , 2000, Anaerobe.

[128]  E. Moore,et al.  Isolation and Identification of Ruminal Methanogens from Grazing Cattle , 2000, Current Microbiology.

[129]  J. Pennings,et al.  Adaptation of methane formation and enzyme contents during growth of Methanobacterium thermoautotrophicum (strain ΔH) in a fed-batch fermentor , 2000, Antonie van Leeuwenhoek.

[130]  Y. Kamagata,et al.  Phylogenetic Analysis of Methanogens in Sheep Rumen Ecosystem and Detection of Methanomicrobium mobile by Fluorescence In Situ Hybridization , 2000, Bioscience, biotechnology, and biochemistry.

[131]  G. B. Fogel,et al.  Prokaryotic Genome Size and SSU rDNA Copy Number: Estimation of Microbial Relative Abundance from a Mixed Population , 1999, Microbial Ecology.

[132]  T. Oshima,et al.  Phylogenetic Diversity of Symbiotic Methanogens Living in the Hindgut of the Lower Termite Reticulitermes speratus Analyzed by PCR and In Situ Hybridization , 1999, Applied and Environmental Microbiology.

[133]  J. Russell,et al.  The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. , 1998, Journal of dairy science.

[134]  S. Ricke,et al.  Induction of Acid Resistance of Salmonella typhimurium by Exposure to Short-Chain Fatty Acids , 1998, Applied and Environmental Microbiology.

[135]  J. Ralph,et al.  Assessment of Reductive Acetogenesis with Indigenous Ruminal Bacterium Populations and Acetitomaculum ruminis , 1998, Applied and Environmental Microbiology.

[136]  J. Russell,et al.  The role of pH in regulating ruminal methane and ammonia production. , 1998, Journal of animal science.

[137]  D. Stahl,et al.  Taxon‐specific associations between protozoal and methanogen populations in the rumen and a model rumen system , 1998 .

[138]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[139]  D. Stahl,et al.  Microbial community structure in gastrointestinal tracts of domestic animals: comparative analyses using rRNA‐targeted oligonucleotide probes , 1997 .

[140]  Rolf K. Thauer Biodiversity and unity in biochemistry , 1997, Antonie van Leeuwenhoek.

[141]  B. B. Jensen Methanogenesis in monogastric animals , 1996, Environmental monitoring and assessment.

[142]  R. Fleischmann,et al.  Complete Genome Sequence of the Methanogenic Archaeon, Methanococcus jannaschii , 1996, Science.

[143]  G. Fonty,et al.  Quantitative Determination of H2-Utilizing Acetogenic and Sulfate-Reducing Bacteria and Methanogenic Archaea from Digestive Tract of Different Mammals , 1996, Current Microbiology.

[144]  Ramaraj Boopathy Isolation and characterization of a methanogenic bacterium from swine manure , 1996 .

[145]  T. Florin,et al.  Inhibition of methanogenesis by human bile. , 1995, Gut.

[146]  Alejandro Grajal,et al.  PASSAGE RATES OF DIGESTA MARKERS IN THE GUT OF THE HOATZIN, A FOLIVOROUS BIRD WITH FOREGUT FERMENTATION' , 1995 .

[147]  D. Johnson,et al.  Methane emissions from cattle. , 1995, Journal of animal science.

[148]  J. Doré,et al.  Enumeration of H2-utilizing methanogenic archaea, acetogenic and sulfate-reducing bacteria from human feces , 1995 .

[149]  T. Kararli Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals , 1995, Biopharmaceutics & drug disposition.

[150]  James G. Ferry,et al.  Methanogenesis : Ecology, Physiology, Biochemistry and Genetics , 1994 .

[151]  P. V. Soest Nutritional Ecology of the Ruminant , 1994 .

[152]  J. Doré,et al.  Establishment of hydrogen-utilizing bacteria in the rumen of the newborn lamb. , 1994, FEMS microbiology letters.

[153]  J. Reeve,et al.  mRNAs in the methanogenic archaeon Methanococcus vannielii: numbers, half‐lives and processing , 1994, Molecular microbiology.

[154]  M. Dominguez-Bello,et al.  Microbial Digestive Symbionts of the Crop of the Hoatzin (Opisthocomus hoazin): An Avian Foregut Fermenter , 1993, Physiological Zoology.

[155]  T. Miller,et al.  Amounts of viable anaerobes, methanogens, and bacterial fermentation products in feces of rats fed high-fiber or fiber-free diets , 1993, Applied and environmental microbiology.

[156]  J. Russell,et al.  Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling , 1992 .

[157]  M. Kane,et al.  Effect of host diet on production of organic acids and methane by cockroach gut bacteria , 1991, Applied and environmental microbiology.

[158]  C. Juste,et al.  Ion-pair high-performance liquid chromatography of bile salt conjugates: Application to pig bile , 1991, Lipids.

[159]  H. Gijzen,et al.  Methanogenic bacteria as endosymbionts of the ciliate Nyctotherus ovalis in the cockroach hindgut , 1991, Applied and environmental microbiology.

[160]  J. Kaneko,et al.  Serum bile acid composition of the dog, cow, horse and human. , 1991, The Journal of veterinary medical science.

[161]  G. Macfarlane,et al.  Alternative pathways for hydrogen disposal during fermentation in the human colon. , 1990, Gut.

[162]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[163]  T. Miller,et al.  Increase in colonic methanogens and total anaerobes in aging rats , 1989, Applied and environmental microbiology.

[164]  D. Wingate Comparative physiology of the vertebrate digestive system , 1989 .

[165]  J. Leedle,et al.  Enumeration of selected anaerobic bacterial groups in cecal and colonic contents of growing-finishing pigs , 1989, Applied and environmental microbiology.

[166]  D. Demeyer,et al.  Fermentation of methanol in the sheep rumen , 1988, Applied and environmental microbiology.

[167]  R. Wolfe,et al.  Nutritional requirements of Methanomicrobium mobile , 1988, Applied and environmental microbiology.

[168]  Ralf Cord-Ruwisch,et al.  The capacity of hydrogenotrophic anaerobic bacteria to compete for traces of hydrogen depends on the redox potential of the terminal electron acceptor , 1988, Archives of Microbiology.

[169]  H. König Chemical composition of cell envelopes of methanogenic bacteria isolated from human and animal feces , 1986 .

[170]  T. Miller,et al.  Methanogens in human and animal intestinal Tracts , 1986 .

[171]  T. Miller,et al.  Enumeration of Methanobrevibacter smithii in human feces , 1982, Archives of Microbiology.

[172]  A. Macario,et al.  Isolation of Methanobrevibacter smithii from human feces , 1982, Applied and environmental microbiology.

[173]  E. Barnes,et al.  Manipulation of the crop and intestinal flora of the newly hatched chick. , 1980, The American journal of clinical nutrition.

[174]  J. Russell,et al.  Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture , 1980, Applied and environmental microbiology.

[175]  C. Woese,et al.  Methanogens: reevaluation of a unique biological group , 1979, Microbiological reviews.

[176]  R. B. Hespell,et al.  Trimethylamine and methylamine as growth substrates for rumen bacteria andMethanosarcina barkeri , 1979, Current Microbiology.

[177]  J. Salanitro,et al.  Bacteria isolated from the duodenum, ileum, and cecum of young chicks , 1978, Applied and environmental microbiology.

[178]  A. R. Neill,et al.  Conversion of choline methyl groups through trimethylamine into methane in the rumen. , 1978, The Biochemical journal.

[179]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[180]  C R Woese,et al.  Classification of methanogenic bacteria by 16S ribosomal RNA characterization. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[181]  R S Wolfe,et al.  New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere , 1976, Applied and environmental microbiology.

[182]  M. P. Bryant,et al.  Commentary on the Hungate technique for culture of anaerobic bacteria. , 1972, The American journal of clinical nutrition.

[183]  R. E. Hungate,et al.  The Roll-Tube Method for Cultivation of Strict Anaerobes , 1972 .

[184]  R. E. Hungate,et al.  Characterization of Methanobacterium mobilis, sp. n., Isolated from the Bovine Rumen , 1968, Journal of bacteriology.

[185]  D. H. Shrimpton Metabolism of the intestinal microflora in birds and its possible influence on the composition of flavour precursors in their muscles. , 1966, The Journal of applied bacteriology.

[186]  P. H. Smith,et al.  ISOLATION AND CHARACTERIZATION OF METHANOBACTERIUM RUMINANTIUM N. SP , 1958, Journal of bacteriology.

[187]  R. E. Hungate,et al.  The anaerobic mesophilic cellulolytic bacteria. , 1950, Bacteriological reviews.

[188]  D. Denbow,et al.  Gastrointestinal Anatomy and Physiology , 2015 .

[189]  U. Gophna,et al.  Contribution of lateral gene transfer to the gene repertoire of a gut-adapted methanogen. , 2012, Genomics.

[190]  Ricardo Cavicchioli,et al.  Archaea — timeline of the third domain , 2011, Nature Reviews Microbiology.

[191]  R. Wolfe Techniques for cultivating methanogens. , 2011, Methods in enzymology.

[192]  S. Ricke,et al.  Prescreening of microbial populations for the assessment of sequencing potential. , 2011, Methods in molecular biology.

[193]  S. Gill,et al.  Phylogenetic analysis of bacterial and archaeal species in symptomatic and asymptomatic endodontic infections. , 2007, Journal of medical microbiology.

[194]  K. Purdy The distribution and diversity of Euryarchaeota in termite guts. , 2007, Advances in applied microbiology.

[195]  D. Gevers,et al.  Phylogenetic and genomic analysis , 2007 .

[196]  A. Mills,et al.  Manual of environmental microbiology. , 2007 .

[197]  C. Sorlini,et al.  Quantitative determination of methanogenic bacteria in the feces of different mammals , 2005, Current Microbiology.

[198]  M. Friedrich Methyl-coenzyme M reductase genes: unique functional markers for methanogenic and anaerobic methane-oxidizing Archaea. , 2005, Methods in enzymology.

[199]  D. Kamra Rumen microbial ecosystem , 2005 .

[200]  James M. Tiedje,et al.  Competition between sulfate-reducing and methanogenic bacteria for H2 under resting and growing conditions , 2004, Archives of Microbiology.

[201]  G. Muyzer,et al.  Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology , 2004, Antonie van Leeuwenhoek.

[202]  Moselio Schaechter,et al.  Desk encyclopedia of microbiology , 2004 .

[203]  U. Deppenmeier The unique biochemistry of methanogenesis. , 2002, Progress in nucleic acid research and molecular biology.

[204]  S. Shima,et al.  Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. , 2002, Journal of bioscience and bioengineering.

[205]  G. Garrity Bergey's Manual of systematic bacteriology , 2001 .

[206]  John L. Howland,et al.  The Surprising Archaea: Discovering Another Domain of Life , 2000 .

[207]  J. Hackstein,et al.  Symbiotic Associations Between Methanogenic Archaea, Protists and Metazoa: Evolutionary Implications , 1999 .

[208]  Joseph Seckbach,et al.  Enigmatic Microorganisms and Life in Extreme Environments , 1999, Cellular Origin and Life in Extreme Habitats.

[209]  S. Ricke,et al.  Ecology, metabolism, and genetics of ruminal selenomonads. , 1996, Critical reviews in microbiology.

[210]  T. Miller Ecology of methane production and hydrogen sinks in the rumen , 1994 .

[211]  Stephen H. Zinder,et al.  Physiological Ecology of Methanogens , 1993 .

[212]  M. Otsuka,et al.  COLONIZATION OF MICROORGANISMS IN THE RUMEN OF YOUNG CALVES , 1992 .

[213]  K. Wood,et al.  Biliary bile acid profiles of domestic fowl as determined by high performance liquid chromatography and fast atom bombardment mass spectrometry. , 1990, Comparative biochemistry and physiology. B, Comparative biochemistry.

[214]  J. Lupton,et al.  Determinants and consequences of colonic luminal pH: implications for colon cancer. , 1990, Nutrition and cancer.

[215]  G. Mead Microbes of the avian cecum: types present and substrates utilized. , 1989, The Journal of experimental zoology. Supplement : published under auspices of the American Society of Zoologists and the Division of Comparative Physiology and Biochemistry.

[216]  K. Fiebig,et al.  Utilization of trimethylamine and other N-methyl compounds for growth and methane formation by Methanosarcina barkeri. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[217]  L. B. Halstead The evolution of the mammals , 1978 .

[218]  R. E. Hungate Chapter IV A Roll Tube Method for Cultivation of Strict Anaerobes , 1969 .

[219]  R. E. Hungate CHAPTER VII – Conversions of Nitrogenous Materials , 1966 .