Erratum: Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range

Ruminant livestock are important sources of human food and global greenhouse gas emissions. Feed degradation and methane formation by ruminants rely on metabolic interactions between rumen microbes and affect ruminant productivity. Rumen and camelid foregut microbial community composition was determined in 742 samples from 32 animal species and 35 countries, to estimate if this was influenced by diet, host species, or geography. Similar bacteria and archaea dominated in nearly all samples, while protozoal communities were more variable. The dominant bacteria are poorly characterised, but the methanogenic archaea are better known and highly conserved across the world. This universality and limited diversity could make it possible to mitigate methane emissions by developing strategies that target the few dominant methanogens. Differences in microbial community compositions were predominantly attributable to diet, with the host being less influential. There were few strong co-occurrence patterns between microbes, suggesting that major metabolic interactions are non-selective rather than specific.

Min Wang | Bo Lin | Chris McSweeney | William J. Kelly | Bostjan Murovec | Itzhak Mizrahi | Graeme T. Attwood | André Bannink | Tasia M. Taxis | William R. Lamberson | Siva Ganesh | Pablo Zunino | Satoshi Koike | Peter H. Janssen | Blaz Stres | Morten Poulsen | Tianhai Yan | Tim A. McAllister | Carl J. Yeoman | Mi Zhou | Le Luo Guan | Jan Dijkstra | Edenio Detmann | Eva Lewis | Jan Lassen | Mads F. Bertelsen | Juha Kantanen | Yasuo Kobayashi | Ilma Tapio | Gemma Henderson | Florian Leiber | Michael O’Donovan | Min Wang | P. B. Pope | I. Mizrahi | J. Šimůnek | M. Bertelsen | S. Ospina | S. Koike | C. Yeoman | J. Newbold | Yasuo Kobayashi | F. Sales | T. Yan | J. Dijkstra | E. Minnee | G. Waghorn | W. Young | P. Janssen | S. Ganesh | J. Kantanen | A. Bannink | Sang-Suk Lee | T. Mcallister | Alexandre B. de Menezes | Dragana Gagic | J. V. Van Hamme | L. Guan | B. Stres | S. Ishaq | C. McSweeney | L. Cersosimo | M. Lachman | W. Kelly | S. Leahy | G. Attwood | E. Hernandez-Sanabria | S. Waters | I. Tapio | M. Witzig | M. Rodehutscord | M. Mitsumori | R. Valizadeh | C. Pinares-Patiño | M. Poulsen | E. Ungerfeld | N. Tomkins | T. Taxis | Rolando Barahona | Torsten Nygaard Kristensen | M. O'Donovan | N. Fukuma | G. Henderson | F. Cox | A. Jonker | L. Abecia | E. Angarita | P. Aravena | Graciela Nora Arenas | C. Ariza | Jose Mauricio Avila | J. Ávila-Stagno | Mariano Batistotti | Aya Brown-Kav | A. Carvajal | Alexandre Vieira Chaves | J. Church | N. Clipson | M. Cobos-Peralta | A. Cookson | S. Cravero | Omar Cristobal Carballo | Katie Crosley | Gustavo Cruz | M. Cerón Cucchi | Rodrigo de la Barra | E. Detmann | K. Dieho | William L. S. dos Reis | M. Dugan | Seyed Hadi Ebrahimi | E. Eythórsdóttir | Fabian Nde Fon | M. Fraga | F. Franco | Chris Friedeman | I. Gangnat | Diego Javier Grilli | Vahideh Heidarian Miri | Alma Ximena Ibarra Gomez | O. A. Isah | E. Jami | J. Jelincic | Seon-Ho Kim | A. Klieve | J. Kopečný | Sophie Julie Krizsan | H. Lachance | W. Lamberson | S. Lambie | J. Lassen | F. Leiber | E. Lewis | Bo Lin | R. Lira | P. Lund | Edgar Macipe | L. Mamuad | Hilário Cuquetto Mantovani | G. Marcoppido | C. Márquez | Cécile Martin | G. Martínez | M. Eugenia Martinez | Olga Lucía Mayorga | L. Mestre | Isabel Molina | A. Muenger | C. Muñoz | Boštjan Murovec | V. Nsereko | S. Okunade | B. O’Neill | D. Ouwerkerk | D. Parra | L. R. Pereira | Tatiana Rodriguez | Kunihiko Saito | Catherine Sauer | K. Shingfield | N. Shoji | Z. Stojanovic-Radic | Xuezhao Sun | J. Swartz | Zhi Liang Tan | P. van Adrichem | W. Van Hoven | R. John Wallace | K. Keogh | A. Wright | Hidehisa Yamano | D. Yáñez-Ruiz | Ricardo Zambrano | J. Zeitz | Mi Zhou | Hua Wei Zhou | Cai Xia Zou | P. Zunino | Nicholas Clipson | Reza Valizadeh | Faith Cox | Jiri Simunek | Arjan Jonker | Wayne Young | Leticia Abecia | Erika Angarita | Paula Aravena | Graciela Nora Arenas | Claudia Ariza | Jose Mauricio Avila | Jorge Avila-Stagno | Rolando Barahona | Mariano Batistotti | Aya Brown-Kav | Andres M. Carvajal | Laura Cersosimo | Alexandre Vieira Chaves | John Church | Mario A. Cobos-Peralta | Adrian L. Cookson | Silvio Cravero | Omar Cristobal Carballo | Katie Crosley | Gustavo Cruz | María Cerón Cucchi | Rodrigo de la Barra | Alexandre B. De Menezes | Kasper Dieho | Mike E. R. Dugan | Seyed Hadi Ebrahimi | Emma Eythórsdóttir | Fabian Nde Fon | Martín Fraga | Francisco Franco | Chris Friedeman | Naoki Fukuma | Dragana Gagić | Isabelle Gangnat | Diego Javier Grilli | Vahideh Heidarian Miri | Emma Hernandez-Sanabria | Olubukola A. Isah | Suzanne Ishaq | Elie Jami | Juan Jelincic | Seon-Ho Kim | Athol Klieve | Jan Kopecny | Torsten Nygaard Kristensen | Sophie Julie Krizsan | Hannah LaChance | Medora Lachman | Suzanne Lambie | Sinead C. Leahy | Sang-Suk Lee | Raúl Lira | Peter Lund | Edgar Macipe | Lovelia L. Mamuad | Hilário Cuquetto Mantovani | Gisela Ariana Marcoppido | Cristian Márquez | Cécile Martin | Gonzalo Martinez | Maria Eugenia Martinez | Olga Lucía Mayorga | Lorena Mestre | Elena Minnee | Makoto Mitsumori | Isabel Molina | Andreas Muenger | Camila Munoz | John Newbold | Victor Nsereko | Sunday Okunade | Brendan O’Neill | Sonia Ospina | Diane Ouwerkerk | Diana Parra | Luiz Gustavo Ribeiro Pereira | Cesar Pinares-Patino | Phil B. Pope | Markus Rodehutscord | Tatiana Rodriguez | Kunihiko Saito | Francisco Sales | Catherine Sauer | Kevin Shingfield | Noriaki Shoji | Zorica Stojanović-Radić | Xuezhao Sun | Jeffery Swartz | Zhi Liang Tan | Nigel Tomkins | Emilio Ungerfeld | Peter van Adrichem | Jonathan Van Hamme | Woulter Van Hoven | Garry Waghorn | R. John Wallace | Sinéad M. Waters | Kate Keogh | Maren Witzig | Andre-Denis G. Wright | Hidehisa Yamano | David R. Yanez-Ruiz | Ricardo Zambrano | Johanna Zeitz | Hua Wei Zhou | Cai Xia Zou | P. Pope | T. McAllister | Y. Kobayashi | A. D. de Menezes | M. Zhou | M. C. Ceron Cucchi | G. Martinez | C. Sauer | Z. Stojanović-Radić | Elie Jami | Faith Cox

[1]  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.

[2]  D. Kenny,et al.  Effect of Phenotypic Residual Feed Intake and Dietary Forage Content on the Rumen Microbial Community of Beef Cattle , 2012, Applied and Environmental Microbiology.

[3]  Itzhak Mizrahi,et al.  Potential Role of the Bovine Rumen Microbiome in Modulating Milk Composition and Feed Efficiency , 2014, PloS one.

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

[5]  S. Kittelmann,et al.  Characterization of rumen ciliate community composition in domestic sheep, deer, and cattle, feeding on varying diets, by means of PCR-DGGE and clone libraries. , 2011, FEMS microbiology ecology.

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

[7]  P. Weimer Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations , 2015, Front. Microbiol..

[8]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[9]  Siva Ganesh,et al.  Two Different Bacterial Community Types Are Linked with the Low-Methane Emission Trait in Sheep , 2014, PloS one.

[10]  Jonathan Friedman,et al.  Inferring Correlation Networks from Genomic Survey Data , 2012, PLoS Comput. Biol..

[11]  Gemma Henderson,et al.  Determining the culturability of the rumen bacterial microbiome , 2014, Microbial biotechnology.

[12]  A. Macpherson,et al.  Interactions Between the Microbiota and the Immune System , 2012, Science.

[13]  H. Seedorf,et al.  Few Highly Abundant Operational Taxonomic Units Dominate within Rumen Methanogenic Archaeal Species in New Zealand Sheep and Cattle , 2014, Applied and Environmental Microbiology.

[14]  Peter H. Janssen,et al.  Effect of DNA Extraction Methods and Sampling Techniques on the Apparent Structure of Cow and Sheep Rumen Microbial Communities , 2013, PloS one.

[15]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[16]  Franz Rubel,et al.  Observed and projected climate shifts 1901-2100 depicted by world maps of the Köppen-Geiger climate classification , 2010 .

[17]  G. Waghorn,et al.  Nitrogen metabolism and rumen microbial enumeration in lactating cows with divergent residual feed intake fed high-digestibility pasture. , 2012, Journal of dairy science.

[18]  T. Hackmann,et al.  Invited review: ruminant ecology and evolution: perspectives useful to ruminant livestock research and production. , 2010, Journal of dairy science.

[19]  A. Mackenzie,et al.  Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation? , 2014, mBio.

[20]  T. Miller,et al.  Methanosphaera stadtmaniae gen. nov., sp. nov.: a species that forms methane by reducing methanol with hydrogen , 1985, Archives of Microbiology.

[21]  J. Russell,et al.  Factors That Alter Rumen Microbial Ecology , 2001, Science.

[22]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[23]  Eric P. Nawrocki,et al.  An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea , 2011, The ISME Journal.

[24]  S. Gribaldo,et al.  Comparative genomics highlights the unique biology of Methanomassiliicoccales, a Thermoplasmatales-related seventh order of methanogenic archaea that encodes pyrrolysine , 2014, BMC Genomics.

[25]  M. P. Bryant,et al.  CHARACTERISTICS OF TWO NEW GENERA OF ANAEROBIC CURVED RODS ISOLATED FROM THE RUMEN OF CATTLE , 1956, Journal of bacteriology.

[26]  S. Kittelmann,et al.  Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium. , 2011, Journal of microbiological methods.

[27]  H. Bohlken REMARKS ON THE STOMACH AND THE SYSTEMATIC POSITION OF THE TYLOPODA , 2009 .

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

[29]  G. Coleman,et al.  The Rumen Protozoa , 1992, Brock/Springer Series in Contemporary Bioscience.

[30]  D. Johnson,et al.  Estimates of animal methane emissions , 1996, Environmental monitoring and assessment.

[31]  B. A. Dehority Pectin-fermenting Bacteria Isolated from the Bovine Rumen , 1969, Journal of bacteriology.

[32]  H. Strobel Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23 , 1992, Applied and environmental microbiology.

[33]  H. Seedorf,et al.  Distributed under Creative Commons Cc-by 4.0 Rim-db: a Taxonomic Framework for Community Structure Analysis of Methanogenic Archaea from the Rumen and Other Intestinal Environments , 2022 .

[34]  G. Wiggans,et al.  The measurement of liquid and solid digesta retention in ruminants, equines and rabbits given timothy (Phleum pratense) hay , 1982, British Journal of Nutrition.

[35]  Thomas Huber,et al.  Bellerophon: a program to detect chimeric sequences in multiple sequence alignments , 2004, Bioinform..

[36]  P. B. Pope,et al.  Metagenomics of the Svalbard Reindeer Rumen Microbiome Reveals Abundance of Polysaccharide Utilization Loci , 2012, PloS one.

[37]  Alfons J. M. Stams,et al.  Electron transfer in syntrophic communities of anaerobic bacteria and archaea , 2009, Nature Reviews Microbiology.

[38]  P. Janssen,et al.  RUMINANT NUTRITION SYMPOSIUM: Use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis. , 2015, Journal of animal science.

[39]  Natalia N. Ivanova,et al.  The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist , 2011, PloS one.

[40]  R. Hofmann Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system , 1989, Oecologia.

[41]  Pete Smith,et al.  Ruminants, climate change and climate policy , 2014 .

[42]  J. Jouany,et al.  The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro , 1995, Letters in applied microbiology.

[43]  Eoin L. Brodie,et al.  Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows , 2011, The ISME Journal.

[44]  I. Koppová,et al.  Relation between phylogenetic position, lipid metabolism and butyrate production by different Butyrivibrio-like bacteria from the rumen , 2007, Antonie van Leeuwenhoek.

[45]  Scott Federhen,et al.  Type material in the NCBI Taxonomy Database , 2014, Nucleic Acids Res..

[46]  Zhongtang Yu,et al.  Status of the phylogenetic diversity census of ruminal microbiomes. , 2011, FEMS microbiology ecology.

[47]  T. Shinkai,et al.  Effect of media composition, including gelling agents, on isolation of previously uncultured rumen bacteria , 2013, Letters in applied microbiology.

[48]  A. Takenaka,et al.  Real-Time PCR Detection of the Effects of Protozoa on Rumen Bacteria in Cattle , 2006, Current Microbiology.