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The rumen microbiome: balancing food security and environmental impacts

Abstract

Ruminants produce edible products and contribute to food security. They house a complex rumen microbial community that enables the host to digest their plant feed through microbial-mediated fermentation. However, the rumen microbiome is also responsible for the production of one of the most potent greenhouse gases, methane, and contributes about 18% of its total anthropogenic emissions. Conventional methods to lower methane production by ruminants have proved successful, but to a limited and often temporary extent. An increased understanding of the host–microbiome interactions has led to the development of new mitigation strategies. In this Review we describe the composition, ecology and metabolism of the rumen microbiome, and the impact on host physiology and the environment. We also discuss the most pertinent methane mitigation strategies that emerged to balance food security and environmental impacts.

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Fig. 1: Global methane emissions.
Fig. 2: Overview of the most prevalent rumen microbiome core members.
Fig. 3: Overview of rumen microbiome metabolism.
Fig. 4: Methane mitigation strategies.

References

  1. 1.

    Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R. & Gordon, J. I. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat. Rev. Microbiol. 6, 776–788 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. 2.

    Mizrahi, I. in The Prokaryotes (eds Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E. & Thompson, F.) 533–544 (Springer, 2013).

  3. 3.

    Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39, 31–40 (2007).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Luckey, T. Germfree Life and Gnotobiology (Elsevier, 2012).

  5. 5.

    Hobson, P. N. & Stewart, C. S. The Rumen Microbial Ecosystem (Springer Science & Business Media, 2012).

  6. 6.

    Lin, L. et al. Ruminal microbiome–host crosstalk stimulates the development of the ruminal epithelium in a lamb model. Microbiome 7, 83 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Mizrahi, I. & Jami, E. Review: The compositional variation of the rumen microbiome and its effect on host performance and methane emission. Animal. 12, s220–s232 (2018).

    CAS  PubMed  Article  Google Scholar 

  8. 8.

    Malmuthuge, N., Liang, G. & Guan, L. L. Regulation of rumen development in neonatal ruminants through microbial metagenomes and host transcriptomes. Genome Biol. 20, 172 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  9. 9.

    Eshel, G., Shepon, A., Makov, T. & Milo, R. Land, irrigation water, greenhouse gas, and reactive nitrogen burdens of meat, eggs, and dairy production in the United States. Proc. Natl Acad. Sci. USA 111, 11996–12001 (2014).

    CAS  PubMed  Article  Google Scholar 

  10. 10.

    Maasakkers, J. D. et al. Global distribution of methane emissions, emission trends, and OH concentrations and trends inferred from an inversion of GOSAT satellite data for 2010–2015. Atmos. Chem. Phys. 19, 7859–7881 (2019).

    CAS  Article  Google Scholar 

  11. 11.

    Dong, H. et al. Emissions from livestock and manure management. Embrapa Meio Ambiente-Capítulo em Livro Científico (ALICE) Vol. 4, 1–87 (iGES, Kanagawa, 2006).

  12. 12.

    Le Quéré, C. et al. Global carbon budget 2018. Earth Syst. Sci. Data 10, 2141–2194 (2018).

    Article  Google Scholar 

  13. 13.

    Huws, S. A. et al. Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future. Front. Microbiol. 9, 2161 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Shabat, S. K. B. et al. Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants. ISME J. 10, 2958–2972 (2016). This study links the compositional states of the cow rumen microbiome to feed efficiency and methane emission, with an emphasis on microbial lactic acid and hydrogen metabolism.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Shaani, Y., Zehavi, T., Eyal, S., Miron, J. & Mizrahi, I. Microbiome niche modification drives diurnal rumen community assembly, overpowering individual variability and diet effects. ISME J. 12, 2446–2457 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Friedman, N., Shriker, E. & Gold, B. Diet-induced changes of redox potential underlie compositional shifts in the rumen archaeal community. Environ. Microbiol. 19, 174–184 (2017).

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Sasson, G. et al. Heritable bovine rumen bacteria are phylogenetically related and correlated with the cow’s capacity to harvest energy from its feed. mBio 8, e00703-17 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Friedman, N., Jami, E. & Mizrahi, I. Compositional and functional dynamics of the bovine rumen methanogenic community across different developmental stages. Environ. Microbiol. 19, 3365–3373 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Li, F. et al. Host genetics influence the rumen microbiota and heritable rumen microbial features associate with feed efficiency in cattle. Microbiome 7, 92 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Li, F., Hitch, T. C. A., Chen, Y., Creevey, C. J. & Guan, L. L. Comparative metagenomic and metatranscriptomic analyses reveal the breed effect on the rumen microbiome and its associations with feed efficiency in beef cattle. Microbiome 7, 6 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  21. 21.

    Nkrumah, J. D. et al. Relationships of feedlot feed efficiency, performance, and feeding behavior with metabolic rate, methane production, and energy partitioning in beef cattle. J. Anim. Sci. 84, 145–153 (2006).

    Article  Google Scholar 

  22. 22.

    Mizrahi, I. in Beneficial Microorganisms in Multicellular Life Forms (eds Rosenberg, E. & Gophna, U.) 203–210 (Springer, 2012).

  23. 23.

    Hart, E. H., Creevey, C. J., Hitch, T. & Kingston-Smith, A. H. Meta-proteomics of rumen microbiota indicates niche compartmentalisation and functional dominance in a limited number of metabolic pathways between abundant bacteria. Sci. Rep. 8, 10501 (2018).

    Article  CAS  Google Scholar 

  24. 24.

    Snelling, T. J. & Wallace, R. J. The rumen microbial metaproteome as revealed by SDS-PAGE. BMC Microbiol. 17, 9 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  25. 25.

    Jami, E. & Mizrahi, I. Composition and similarity of bovine rumen microbiota across individual animals. PLoS ONE 7, e33306 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Morais, S. & Mizrahi, I. Islands in the stream: from individual to communal fiber degradation in the rumen ecosystem. FEMS Rev. Microbiol. 43, 362–379 (2019). This review summarizes the enzymological fundamentals of fibre degradation with an emphasis on the community perspective, from individual genetic information to microbial interactions.

    CAS  Article  Google Scholar 

  27. 27.

    Henderson, G. et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci. Rep. 5, 14567 (2015). This important study defines the rumen core microbiome across ruminant species with relation to geography and diet.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Wallace, R. J. et al. A heritable subset of the core rumen microbiome dictates dairy cow productivity and emissions. Sci. Adv. 5, eaav8391 (2019). This 1,000-animal study provides deep understanding of the extent to which ruminant microbiomes can be controlled by the host animal. The study identifies the characteristics of the host rumen microbiome axis that determine animal productivity and methane emissions.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Huws, S. A. et al. Temporal dynamics of the metabolically active rumen bacteria colonizing fresh perennial ryegrass. FEMS Microbiol. Ecol. 92, fiv137 (2016).

    PubMed  Article  CAS  Google Scholar 

  30. 30.

    Piao, H. et al. Temporal dynamics of fibrolytic and methanogenic rumen microorganisms during in situ incubation of switchgrass determined by 16S rRNA gene profiling. Front. Microbiol. 5, 307 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Liu, J., Zhang, M., Xue, C., Zhu, W. & Mao, S. Characterization and comparison of the temporal dynamics of ruminal bacterial microbiota colonizing rice straw and alfalfa hay within ruminants. J. Dairy. Sci. 99, 9668–9681 (2016).

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Jin, W., Wang, Y., Li, Y., Cheng, Y. & Zhu, W. Temporal changes of the bacterial community colonizing wheat straw in the cow rumen. Anaerobe 50, 1–8 (2018).

    PubMed  Article  Google Scholar 

  33. 33.

    Stanton, T. B. & Canale-Parola, E. Treponema bryantii sp. nov., a rumen spirochete that interacts with cellulolytic bacteria. Arch. Microbiol. 127, 145–156 (1980).

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Blackburn, T. H. & Hungate, R. E. Succinic acid turnover and propionate production in the bovine rumen. Appl. Microbiol. 11, 132–135 (1963).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Scheifinger, C. C. & Wolin, M. J. Propionate formation from cellulose and soluble sugars by combined cultures of Bacteroides succinogenes and Selenomonas ruminantium. Appl. Microbiol. 26, 789–795 (1973).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Kim, M., Morrison, M. & Yu, Z. Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol. Ecol. 76, 49–63 (2011).

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Arntzen, M. Ø., Várnai, A., Mackie, R. I., Eijsink, V. G. H. & Pope, P. B. Outer membrane vesicles from Fibrobacter succinogenes S85 contain an array of carbohydrate-active enzymes with versatile polysaccharide-degrading capacity. Environ. Microbiol. 19, 2701–2714 (2017).

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Suen, G. et al. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLoS ONE 6, e18814 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    O’Hara, E. et al. Investigating temporal microbial dynamics in the rumen of beef calves raised on two farms during early life. FEMS Microbiol. Ecol. 96, fiz203 (2020).

    PubMed  Article  CAS  Google Scholar 

  40. 40.

    Furman, O. et al. Stochasticity constrained by deterministic effects of diet and age drive rumen microbiome assembly dynamics. Nat. Commun. 11, 1904 (2020). This study demonstrates that stochastic colonization in early life, together with strong deterministic constraints imposed by diet and age, exhibits long-lasting impact on the development of animal microbiomes.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. 41.

    Moraïs, S. & Mizrahi, I. The road not taken: the rumen microbiome, functional groups, and community states. Trends Microbiol. 27, 538–549 (2019). This review takes an ecological approach to introduce the concept of the rumen functional group and community states to guide the interpretation of rumen microbiome data.

    PubMed  Article  CAS  Google Scholar 

  42. 42.

    Weimer, P. J. Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Front. Microbiol. 6, 296 (2015). This excellent review provides an ecological perspective of rumen metabolism.

    PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Seshadri, R. et al. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat. Biotechnol. 36, 359–367 (2018). This fundamental publication describes the genome resource of the Hungate1000 rumen isolates.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Taxis, T. M. et al. The players may change but the game remains: network analyses of ruminal microbiomes suggest taxonomic differences mask functional similarity. Nucleic Acids Res. 43, 9600–9612 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Hackmann, T. J., Ngugi, D. K. & Firkins, J. L. Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids. Environmentalist 19, 4670–4683 (2017).

    CAS  Google Scholar 

  46. 46.

    Matte, A., Forsberg, C. W. & Verrinder Gibbins, A. M. Enzymes associated with metabolism of xylose and other pentoses by Prevotella (Bacteroides) ruminicola strains, Selenomonas ruminantium D, and Fibrobacter succinogenes S85. Can. J. Microbiol. 38, 370–S376 (1992).

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Louis, P. & Flint, H. J. Formation of propionate and butyrate by the human colonic microbiota. Environ. Microbiol. 19, 29–41 (2017).

    CAS  PubMed  Article  Google Scholar 

  48. 48.

    Reichardt, N. et al. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME J. 8, 1323–1335 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Laverde Gomez, J. A. et al. Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria. Environ. Microbiol. 21, 259–271 (2019).

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Le Van, T. D. et al. Assessment of reductive acetogenesis with indigenous ruminal bacterium populations and Acetitomaculum ruminis. Appl. Environ. Microbiol. 64, 3429–3436 (1998).

    PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Fonty, G. et al. Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs. Appl. Environ. Microbiol. 73, 6391–6403 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Valdés, C., Newbold, C. J., Hillman, K. & Wallace, R. J. Evidence for methane oxidation in rumen fluid in vitro. Ann. Zootech. 45, 351–351 (1996).

    Article  Google Scholar 

  53. 53.

    Janssen, P. H. & Kirs, M. Structure of the archaeal community of the rumen. Appl. Environ. Microbiol. 74, 3619–3625 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Demirel, B. & Scherer, P. The roles of acetotrophic and hydrogenotrophic methanogens during anaerobic conversion of biomass to methane: a review. Rev. Environ. Sci. Technol. 7, 173–190 (2008).

    CAS  Google Scholar 

  55. 55.

    Ferry, J. G. Enzymology of one-carbon metabolism in methanogenic pathways. FEMS Microbiol. Rev. 23, 13–38 (1999).

    CAS  PubMed  Article  Google Scholar 

  56. 56.

    Morgavi, D. P., Forano, E., Martin, C. & Newbold, C. J. Microbial ecosystem and methanogenesis in ruminants. Animal 4, 1024–1036 (2010).

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    Guzman, C. E., Bereza-Malcolm, L. T., De Groef, B. & Franks, A. E. Presence of selected methanogens, fibrolytic bacteria, and proteobacteria in the gastrointestinal tract of neonatal dairy calves from birth to 72 hours. PLoS ONE 10, e0133048 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  58. 58.

    Friedman, N., Jami, E. & Mizrahi, I. Compositional and functional dynamics of the bovine rumen methanogenic community across different developmental stages. Environ. Microbiol. 19, 3365–3373 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. 59.

    Flint, H. J. The rumen microbial ecosystem — some recent developments. Trends Microbiol. 5, 483–488 (1997).

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Greening, C. et al. Diverse hydrogen production and consumption pathways influence methane production in ruminants. ISME J. 13, 2617–2632 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. 61.

    Janssen, P. H. Influence of hydrogen on rumen methane formation and fermentation balances through microbial growth kinetics and fermentation thermodynamics. Anim. Feed. Sci. Technol. 160, 1–22 (2010).

    CAS  Article  Google Scholar 

  62. 62.

    Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7, 568–577 (2009).

    CAS  PubMed  Article  Google Scholar 

  63. 63.

    Latham, M. J. & Wolin, M. J. Fermentation of cellulose by Ruminococcus flavefaciens in the presence and absence of Methanobacterium ruminantium. Appl. Environ. Microbiol. 34, 297–301 (1977).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Thauer, R. K., Jungermann, K. & Decker, K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100 (1977).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. 65.

    Bauchop, T. & Mountfort, D. O. Cellulose fermentation by a rumen anaerobic fungus in both the absence and the presence of rumen methanogens. Appl. Environ. Microbiol. 42, 1103–1110 (1981).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. 66.

    Rychlik, J. L. & May, T. The effect of a methanogen, Methanobrevibacter smithii, on the growth rate, organic acid production, and specific ATP activity of three predominant ruminal cellulolytic bacteria. Curr. Microbiol. 40, 176–180 (2000).

    CAS  PubMed  Article  Google Scholar 

  67. 67.

    Leahy, S. C. et al. The genome sequence of the rumen methanogen Methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS ONE 5, e8926 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  68. 68.

    Scheifinger, C. C., Linehan, B. & Wolin, M. J. H2 production by Selenomonas ruminantium in the absence and presence of methanogenic bacteria. Appl. Microbiol. 29, 480–483 (1975).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Cazier, E. A., Trably, E., Steyer, J. P. & Escudie, R. Biomass hydrolysis inhibition at high hydrogen partial pressure in solid-state anaerobic digestion. Bioresour. Technol. 190, 106–113 (2015).

    CAS  PubMed  Article  Google Scholar 

  70. 70.

    Morvan, B., Bonnemoy, F., Fonty, G. & Gouet, P. Quantitative determination of H2-utilizing acetogenic and sulfate-reducing bacteria and methanogenic archaea from digestive tract of different mammals. Curr. Microbiol. 32, 129–133 (1996).

    CAS  PubMed  Article  Google Scholar 

  71. 71.

    Newbold, C. J., de la Fuente, G., Belanche, A., Ramos-Morales, E. & McEwan, N. R. The role of ciliate protozoa in the rumen. Front. Microbiol. 6, 1313 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  72. 72.

    Ushida, K., Newbold, C. J. & Jouany, J.-P. Interspecies hydrogen transfer between the rumen ciliate Polyplastron multivesiculatum and Methanosarcina barkeri. J. Gen. Appl. Microbiol. 43, 129–131 (1997).

    CAS  PubMed  Article  Google Scholar 

  73. 73.

    Wright, A. D. G. & Hook, S. E. 16 Manipulation of microbial ecology for sustainable animal production. Sustain. Anim. Agr. https://doi.org/10.1079/9781780640426.0254254 (2013).

    Article  Google Scholar 

  74. 74.

    Sharp, R., Ziemer, C. J., Stern, M. D. & Stahl, D. A. Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiol. Ecol. 26, 71–78 (1998).

    CAS  Article  Google Scholar 

  75. 75.

    Lloyd, D. et al. Intracellular prokaryotes in rumen ciliate protozoa: detection by confocal laser scanning microscopy after in situ hybridization with fluorescent 16S rRNA probes. Eur. J. Protistol. 32, 523–531 (1996).

    Article  Google Scholar 

  76. 76.

    Ng, F. et al. An adhesin from hydrogen-utilizing rumen methanogen Methanobrevibacter ruminantium M1 binds a broad range of hydrogen-producing microorganisms. Environ. Microbiol. 18, 3010–3021 (2016).

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Zhou, M., Hernandez-Sanabria, E. & Guan, L. L. Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Appl. Environ. Microbiol. 75, 6524–6533 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 78.

    Wallace, R. J. et al. The rumen microbial metagenome associated with high methane production in cattle. BMC Genomics 16, 839 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  79. 79.

    Tapio, I., Snelling, T. J., Strozzi, F. & Wallace, R. J. The ruminal microbiome associated with methane emissions from ruminant livestock. J. Anim. Sci. Biotechnol. 8, 7 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  80. 80.

    Gralka, M., Szabo, R., Stocker, R. & Cordero, O. X. Trophic interactions and the drivers of microbial community assembly. Curr. Biol. 30, R1176–R1188 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  81. 81.

    Kamke, J. et al. Rumen metagenome and metatranscriptome analyses of low methane yield sheep reveals a Sharpea-enriched microbiome characterised by lactic acid formation and utilisation. Microbiome 4, 56 (2016). This study links rumen lactic acid and hydrogen metabolism to methane emissions in sheep.

    PubMed  PubMed Central  Article  Google Scholar 

  82. 82.

    Pope, P. B. et al. Isolation of Succinivibrionaceae implicated in low methane emissions from Tammar wallabies. Science 333, 646–648 (2011).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  83. 83.

    Mi, L. et al. Comparative analysis of the microbiota between sheep rumen and rabbit cecum provides new insight into their differential methane production. Front. Microbiol. 9, 575 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  84. 84.

    Kittelmann, S. et al. Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS ONE 9, e103171 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  85. 85.

    Lee, P. C., Lee, W. G., Kwon, S., Lee, S. Y. & Chang, H. N. Succinic acid production by Anaerobiospirillum succiniciproducens: effects of the H2/CO2 supply and glucose concentration. Enzyme Microb. Technol. 24, 549–554 (1999).

    CAS  Article  Google Scholar 

  86. 86.

    Ungerfeld, E. M. & Kohn, R. A. in Ruminant Physiology: Digestion, Metabolism and Impact of Nutrition on Gene Expression, Immunology and Stress 55–85 (Wageningen Academic, 2006).

  87. 87.

    Shi, W. et al. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Res. 24, 1517–1525 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  88. 88.

    Morgavi, D. P., Martin, C., Jouany, J.-P. & Ranilla, M. J. Rumen protozoa and methanogenesis: not a simple cause–effect relationship. Br. J. Nutr. 107, 388–397 (2012).

    CAS  PubMed  Article  Google Scholar 

  89. 89.

    Grainger, C. & Beauchemin, K. A. Can enteric methane emissions from ruminants be lowered without lowering their production? Anim. Feed. Sci. Technol. 166–167, 308–320 (2011).

    Article  CAS  Google Scholar 

  90. 90.

    Hristov, A. N. et al. An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production. Proc. Natl Acad. Sci. USA 112, 10663–10668 (2015).

    CAS  PubMed  Article  Google Scholar 

  91. 91.

    Ungerfeld, E. M. Shifts in metabolic hydrogen sinks in the methanogenesis-inhibited ruminal fermentation: a meta-analysis. Front. Microbiol. 6, 37 (2015). This report analyses 54 studies on the redirection of hydrogen to potential alternative metabolic sinks when methanogenesis is inhibited.

    PubMed  PubMed Central  Google Scholar 

  92. 92.

    McAllister, T. A. et al. Ruminant nutrition symposium: use of genomics and transcriptomics to identify strategies to lower ruminal methanogenesis. J. Anim. Sci. 93, 1431–1449 (2015).

    CAS  PubMed  Article  Google Scholar 

  93. 93.

    Morgavi, D. P., Kelly, W. J., Janssen, P. H. & Attwood, G. T. Rumen microbial (meta)genomics and its application to ruminant production. Animal 7 (Suppl. 1), 184–201 (2013).

    CAS  PubMed  Article  Google Scholar 

  94. 94.

    Patra, A., Park, T., Kim, M. & Yu, Z. Rumen methanogens and mitigation of methane emission by anti-methanogenic compounds and substances. J. Anim. Sci. Biotechnol. 8, 13 (2017). This article presents a thorough review of methanogens and methane mitigation strategies.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  95. 95.

    Kumar, S. et al. New aspects and strategies for methane mitigation from ruminants. Appl. Microbiol. Biotechnol. 98, 31–44 (2014).

    CAS  PubMed  Article  Google Scholar 

  96. 96.

    Wallace, R. J., Snelling, T. J., McCartney, C. A., Tapio, I. & Strozzi, F. Application of meta-omics techniques to understand greenhouse gas emissions originating from ruminal metabolism. Genet. Sel. Evol. 49, 9 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  97. 97.

    Yang, C., Rooke, J. A., Cabeza, I. & Wallace, R. J. Nitrate and inhibition of ruminal methanogenesis: microbial ecology, obstacles, and opportunities for lowering methane emissions from ruminant livestock. Front. Microbiol. 7, 132 (2016).

    PubMed  PubMed Central  Google Scholar 

  98. 98.

    Martin, C., Morgavi, D. P. & Doreau, M. Methane mitigation in ruminants: from microbe to the farm scale. Animal 4, 351–365 (2010). This article presents a detailed review of methane mitigation approaches.

    CAS  PubMed  Article  Google Scholar 

  99. 99.

    Lan, W. & Yang, C. Ruminal methane production: associated microorganisms and the potential of applying hydrogen-utilizing bacteria for mitigation. Sci. Total. Environ. 654, 1270–1283 (2019).

    CAS  PubMed  Article  Google Scholar 

  100. 100.

    Liu, L. et al. Nitrate decreases methane production also by increasing methane oxidation through stimulating NC10 population in ruminal culture. AMB. Express 7, 76 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  101. 101.

    Yu, Z. & Smith, G. B. Inhibition of methanogenesis by C1-and C2-polychlorinated aliphatic hydrocarbons. Environ. Toxicol. Chem. 19, 2212–2217 (2000).

    CAS  Article  Google Scholar 

  102. 102.

    Wagner, T., Wegner, C.-E., Kahnt, J., Ermler, U. & Shima, S. Phylogenetic and structural comparisons of the three types of methyl coenzyme M reductase from methanococcales and methanobacteriales. J. Bacteriol. 199, e00197-17 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  103. 103.

    Duval, S. & Kindermann, M. Use of nitrooxy organic molecules in feed for reducing enteric methnae emsions in ruminants, and/or to improve ruminant performance. International Patent Application WO 2012/084629 A1 (2012).

  104. 104.

    Burreson, B. J., Moore, R. E. & Roller, P. P. Volatile halogen compounds in the alga Asparagopsis taxiformis (Rhodophyta). J. Agric. Food Chem. 24, 856–861 (1976).

    CAS  Article  Google Scholar 

  105. 105.

    Roque, B. M. et al. Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage. Anim. Microbiome 1, 3 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  106. 106.

    Machado, L. et al. Identification of bioactives from the red seaweed Asparagopsis taxiformis that promote antimethanogenic activity in vitro. J. Appl. Phycol. 28, 3117–3126 (2016).

    CAS  Article  Google Scholar 

  107. 107.

    Knight, T. et al. Chloroform decreases rumen methanogenesis and methanogen populations without altering rumen function in cattle. Anim. Feed. Sci. Technol. 166–167, 101–112 (2011).

    Article  CAS  Google Scholar 

  108. 108.

    Ungerfeld, E. M., Rust, S. R., Boone, D. R. & Liu, Y. Effects of several inhibitors on pure cultures of ruminal methanogens. J. Appl. Microbiol. 97, 520–526 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  109. 109.

    Van Wesemael, D. et al. Reducing enteric methane emissions from dairy cattle: two ways to supplement 3-nitrooxypropanol. J. Dairy Sci. 102, 1780–1787 (2019).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  110. 110.

    Machado, L., Magnusson, M., Paul, N. A., de Nys, R. & Tomkins, N. Effects of marine and freshwater macroalgae on in vitro total gas and methane production. PLoS ONE 9, e85289 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  111. 111.

    Li, X. et al. Asparagopsis taxiformis decreases enteric methane production from sheep. Anim. Prod. Sci. 58, 681 (2018).

    CAS  Article  Google Scholar 

  112. 112.

    Kelly, W. J. et al. The complete genome sequence of the rumen methanogen Methanobacterium formicicum BRM9. Stand. Genomic Sci. 9, 15 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  113. 113.

    Altermann, E., Schofield, L. R., Ronimus, R. S., Beatty, A. K. & Reilly, K. Inhibition of rumen methanogens by a novel archaeal lytic enzyme displayed on tailored bionanoparticles. Front. Microbiol. 9, 2378 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  114. 114.

    Williams, Y. J. et al. A vaccine against rumen methanogens can alter the composition of archaeal populations. Appl. Environ. Microbiol. 75, 1860–1866 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. 115.

    Stewart, R. D. et al. Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery. Nat. Biotechnol. 37, 953–961 (2019). This important resource on rumen microbial genomes enables a better understanding of the structure and function of the rumen microbiota.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. 116.

    Gagen, E. J. et al. Methanogen colonisation does not significantly alter acetogen diversity in lambs isolated 17 h after birth and raised aseptically. Microb. Ecol. 64, 628–640 (2012).

    CAS  PubMed  Article  Google Scholar 

  117. 117.

    Ungerfeld, E. M., Kohn, R. A., Wallace, R. J. & Newbold, C. J. A meta-analysis of fumarate effects on methane production in ruminal batch cultures. J. Anim. Sci. 85, 2556–2563 (2007).

    CAS  PubMed  Article  Google Scholar 

  118. 118.

    Ungerfeld, E. M., Rust, S. R. & Burnett, R. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis. Reprod. Nutr. Dev. 43, 189–202 (2003).

    CAS  PubMed  Article  Google Scholar 

  119. 119.

    van Zijderveld, S. M. et al. Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. J. Dairy Sci. 93, 5856–5866 (2010).

    PubMed  Article  CAS  Google Scholar 

  120. 120.

    Latham, E. A., Anderson, R. C., Pinchak, W. E. & Nisbet, D. J. Insights on alterations to the rumen ecosystem by nitrate and nitrocompounds. Front. Microbiol. 7, 228 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  121. 121.

    Huisingh, J., McNeill, J. J. & Matrone, G. Sulfate reduction by a Desulfovibrio species isolated from sheep rumen. Appl. Microbiol. 28, 489–497 (1974).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. 122.

    Iwamoto, M., Asanuma, N. & Hino, T. Ability of Selenomonas ruminantium, Veillonella parvula, and Wolinella succinogenes to reduce nitrate and nitrite with special reference to the suppression of ruminal methanogenesis. Anaerobe 8, 209–215 (2002).

    CAS  Article  Google Scholar 

  123. 123.

    Kandylis, K. Toxicology of sulfur in ruminants: review. J. Dairy Sci. 67, 2179–2187 (1984).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  124. 124.

    Ungerfeld, E. M. A theoretical comparison between two ruminal electron sinks. Front. Microbiol. 4, 319 (2013). This important study examines and compares the nutritional and energetic implications of directing hydrogen into acetogenesis or propionate production at the expense of methanogenesis.

    PubMed  PubMed Central  Article  Google Scholar 

  125. 125.

    Foley, P. A., Kenny, D. A., Callan, J. J., Boland, T. M. & O’Mara, F. P. Effect of dl-malic acid supplementation on feed intake, methane emission, and rumen fermentation in beef cattle. J. Anim. Sci. 87, 1048–1057 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  126. 126.

    Eugène, M., Massé, D., Chiquette, J. & Benchaar, C. Meta-analysis on the effects of lipid supplementation on methane production in lactating dairy cows. Can. J. Anim. Sci. 88, 331–337 (2008).

    Article  Google Scholar 

  127. 127.

    Patra, A. K. The effect of dietary fats on methane emissions, and its other effects on digestibility, rumen fermentation and lactation performance in cattle: a meta-analysis. Livest. Sci. 155, 244–254 (2013).

    Article  Google Scholar 

  128. 128.

    Belanche, A. et al. A meta-analysis describing the effects of the essential oils blend Agolin ruminant on performance, rumen fermentation and methane emissions in dairy cows. Animals (Basel) 10, 620 (2020).

    Article  Google Scholar 

  129. 129.

    Bergen, W. G. & Bates, D. B. Ionophores: their effect on production efficiency and mode of action. J. Anim. Sci. 58, 1465–1483 (1984).

    CAS  PubMed  Article  Google Scholar 

  130. 130.

    Callaway, T. R. et al. Ionophores: their use as ruminant growth promotants and impact on food safety. Curr. Issues Intest. Microbiol. 4, 43–51 (2003).

    CAS  PubMed  Google Scholar 

  131. 131.

    Maron, D. F., Smith, T. J. S. & Nachman, K. E. Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Global. Health 9, 48 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  132. 132.

    Cotter, P. D., Paul Ross, R. & Hill, C. Bacteriocins — a viable alternative to antibiotics? Nat. Rev. Microbiol. 11, 95–105 (2013).

    CAS  PubMed  Article  Google Scholar 

  133. 133.

    Shen, J., Liu, Z., Yu, Z. & Zhu, W. Monensin and nisin affect rumen fermentation and microbiota differently in vitro. Front. Microbiol. 8, 1111 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  134. 134.

    Lourenço, M., Ramos-Morales, E. & Wallace, R. J. The role of microbes in rumen lipolysis and biohydrogenation and their manipulation. Animal 4, 1008–1023 (2010).

    PubMed  Article  CAS  Google Scholar 

  135. 135.

    Enjalbert, F., Combes, S., Zened, A. & Meynadier, A. Rumen microbiota and dietary fat: a mutual shaping. J. Appl. Microbiol. 123, 782–797 (2017).

    CAS  PubMed  Article  Google Scholar 

  136. 136.

    Lovett, D. et al. Effect of forage/concentrate ratio and dietary coconut oil level on methane output and performance of finishing beef heifers. Livest. Prod. Sci. 84, 135–146 (2003).

    Article  Google Scholar 

  137. 137.

    Prabhu, R., Altman, E. & Eiteman, M. A. Lactate and acrylate metabolism by Megasphaera elsdenii under batch and steady-state conditions. Appl. Environ. Microbiol. 78, 8564–8570 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  138. 138.

    Ungerfeld, E. M. Metabolic hydrogen flows in rumen fermentation: principles and possibilities of interventions. Front. Microbiol. 11, 589 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  139. 139.

    Hristov, A. N. et al. Special topics — Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options. J. Anim. Sci. 91, 5045–5069 (2013).

    CAS  PubMed  Article  Google Scholar 

  140. 140.

    Hook, S. E., Wright, A.-D. G. & McBride, B. W. Methanogens: methane producers of the rumen and mitigation strategies. Archaea 2010, 945785 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  141. 141.

    Goopy, J. P. et al. Low-methane yield sheep have smaller rumens and shorter rumen retention time. Br. J. Nutr. 111, 578–585 (2014).

    CAS  PubMed  Article  Google Scholar 

  142. 142.

    Ørskov, E. R., Ojwang, I. & Reid, G. W. A study on consistency of differences between cows in rumen outflow rate of fibrous particles and other substrates and consequences for digestibility and intake of roughages. Anim. Sci. 47, 45–51 (1988).

    Article  Google Scholar 

  143. 143.

    Herd, R. M. et al. Measures of methane production and their phenotypic relationships with dry matter intake, growth, and body composition traits in beef cattle. J. Anim. Sci. 92, 5267–5274 (2014).

    CAS  PubMed  Article  Google Scholar 

  144. 144.

    Donoghue, K. A., Bird-Gardiner, T. L., Arthur, P. F., Herd, R. M. & Hegarty, R. F. Genetic parameters for methane production and relationships with production traits in Australian beef cattle. Proc. Assoc. Adv. Anim. Breed. Genet. 21, 114–117 (2015).

    Google Scholar 

  145. 145.

    Breider, I. S., Wall, E. & Garnsworthy, P. C. Short communication: Heritability of methane production and genetic correlations with milk yield and body weight in Holstein-Friesian dairy cows. J. Dairy Sci. 102, 7277–7281 (2019).

    CAS  PubMed  Article  Google Scholar 

  146. 146.

    New Zealand Agricultural Greenhouse Gas Research Centre (NZAGRC). Annual Report (2019) 51–59 https://www.nzagrc.org.nz/annualreport,listing,598,annual-report-2019.html (2019).

  147. 147.

    Difford, G. F. et al. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLoS Genet. 14, e1007580 (2018). This study confirms that methane production is influenced by both host genotype and rumen microbiome composition independently from each other.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  148. 148.

    Xiang, R. et al. Gene network analysis identifies rumen epithelial cell proliferation, differentiation and metabolic pathways perturbed by diet and correlated with methane production. Sci. Rep. 6, 39022 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  149. 149.

    Abecia, L., Martín-García, A. I., Martínez, G., Newbold, C. J. & Yáñez-Ruiz, D. R. Nutritional intervention in early life to manipulate rumen microbial colonization and methane output by kid goats postweaning. J. Anim. Sci. 91, 4832–4840 (2013).

    CAS  PubMed  Article  Google Scholar 

  150. 150.

    Abecia, L. et al. Feeding management in early life influences microbial colonisation and fermentation in the rumen of newborn goat kids. Anim. Produc. Sci. 54, 1449–1454 (2014).

    CAS  Article  Google Scholar 

  151. 151.

    Abecia, L. et al. Analysis of the rumen microbiome and metabolome to study the effect of an antimethanogenic treatment applied in early life of kid goats. Front. Microbiol. 9, 2227 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  152. 152.

    Guyader, J. et al. Influence of rumen protozoa on methane emission in ruminants: a meta-analysis approach. Animal 8, 1816–1825 (2014).

    CAS  PubMed  Article  Google Scholar 

  153. 153.

    Morgavi, D. P., Jouany, J. P. & Martin, C. Changes in methane emission and rumen fermentation parameters induced by refaunation in sheep. Aust. J. Exp. Agric. 48, 69–72 (2008).

    CAS  Article  Google Scholar 

  154. 154.

    Belanche, A., de la Fuente, G. & Newbold, C. J. Effect of progressive inoculation of fauna-free sheep with holotrich protozoa and total-fauna on rumen fermentation, microbial diversity and methane emissions. FEMS Microbiol. Ecol. 91, fiu026 (2015).

    PubMed  Article  CAS  Google Scholar 

  155. 155.

    Hegarty, R. S., Bird, S. H., Vanselow, B. A. & Woodgate, R. Effects of the absence of protozoa from birth or from weaning on the growth and methane production of lambs. Br. J. Nutr. 100, 1220–1227 (2008).

    CAS  PubMed  Article  Google Scholar 

  156. 156.

    Hegarty, R. S. Reducing rumen methane emissions through elimination of rumen protozoa. Aust. J. Agric. Res. 50, 1321 (1999).

    Article  Google Scholar 

  157. 157.

    Yáñez-Ruiz, D. R., Abecia, L. & Newbold, C. J. Manipulating rumen microbiome and fermentation through interventions during early life: a review. Front. Microbiol. 6, 1133 (2015). This review presents findings that relate to early-life rumen microbiome development and potential interventions in the process.

    PubMed  PubMed Central  Article  Google Scholar 

  158. 158.

    Jami, E., Israel, A., Kotser, A. & Mizrahi, I. Exploring the bovine rumen bacterial community from birth to adulthood. ISME J. 7, 1069–1079 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  159. 159.

    Zehavi, T., Probst, M. & Mizrahi, I. Insights into culturomics of the rumen microbiome. Front. Microbiol. 9, 1999 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  160. 160.

    Creevey, C. J., Kelly, W. J., Henderson, G. & Leahy, S. C. Determining the culturability of the rumen bacterial microbiome. Microb. Biotechnol. 7, 467–479 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  161. 161.

    Levy, B. & Jami, E. Exploring the prokaryotic community associated with the rumen ciliate protozoa population. Front. Microbiol. 9, 2526 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  162. 162.

    Lima, F. S. et al. Prepartum and postpartum rumen fluid microbiomes: characterization and correlation with production traits in dairy cows. Appl. Environ. Microbiol. 81, 1327–1337 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  163. 163.

    Petri, R. M. et al. Characterization of the core rumen microbiome in cattle during transition from forage to concentrate as well as during and after an acidotic challenge. PLoS ONE 8, e83424 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  164. 164.

    Wu, S., Baldwin, R. L., Li, W., Li, C. & Li, R. W. The bacterial community composition of the bovine rumen detected using pyrosequencing of 16S rRNA genes. Metagenomics 1, 1–11 (2012).

    Article  Google Scholar 

  165. 165.

    Hughes, P. & Heritage, J. Antibiotic growth-promoters in food animals. FAO Anim. Prod. Health Pap. 160, 129–152 (2004).

    Google Scholar 

  166. 166.

    European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA) & European Medicines Agency (EMA). ECDC/EFSA/EMA second joint report on the integrated analysis of the consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals. EFSA J. 15, e04872 (2017).

  167. 167.

    Van Boeckel, T. P. et al. Global trends in antimicrobial use in food animals. Proc. Natl Acad. Sci. USA 112, 5649–5654 (2015).

    PubMed  Article  CAS  Google Scholar 

  168. 168.

    Landers, T. F., Cohen, B., Wittum, T. E. & Larson, E. L. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep. 127, 4–22 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  169. 169.

    Cuong, N. V., Padungtod, P., Thwaites, G. & Carrique-Mas, J. J. Antimicrobial usage in animal production: a review of the literature with a focus on low- and middle-income countries. Antibiotics (Basel) 7, 75 (2018).

    Article  Google Scholar 

  170. 170.

    Shterzer, N. & Mizrahi, I. The animal gut as a melting pot for horizontal gene transfer. Can. J. Microbiol. 61, 603–605 (2015).

    CAS  PubMed  Article  Google Scholar 

  171. 171.

    Kav, A. B. et al. Insights into the bovine rumen plasmidome. Proc. Natl Acad. Sci. USA 109, 5452–5457 (2012).

    CAS  Article  Google Scholar 

  172. 172.

    Sabino, Y. N. V. et al. Characterization of antibiotic resistance genes in the species of the rumen microbiota. Nat. Commun. 10, 5252 (2019).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  173. 173.

    Brown Kav, A. et al. Unravelling plasmidome distribution and interaction with its hosting microbiome. Environ. Microbiol. 22, 32–44 (2020).

    PubMed  Article  Google Scholar 

  174. 174.

    Auffret, M. D. et al. The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle. Microbiome 5, 159 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  175. 175.

    Noyes, N. R. et al. Characterization of the resistome in manure, soil and wastewater from dairy and beef production systems. Sci. Rep. 6, 24645 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  176. 176.

    Thomas, M. et al. Metagenomic characterization of the effect of feed additives on the gut microbiome and antibiotic resistome of feedlot cattle. Sci. Rep. 7, 12257 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  177. 177.

    Chambers, L. et al. Metagenomic analysis of antibiotic resistance genes in dairy cow feces following therapeutic administration of third generation cephalosporin. PLoS ONE 10, e0133764 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  178. 178.

    Cameron, A. & McAllister, T. A. Antimicrobial usage and resistance in beef production. J. Anim. Sci. Biotechnol. 7, 68 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  179. 179.

    Muurinen, J. et al. Influence of manure application on the environmental resistome under Finnish agricultural practice with restricted antibiotic use. Environ. Sci. Technol. 51, 5989–5999 (2017).

    CAS  PubMed  Article  Google Scholar 

  180. 180.

    Tripathi, V. & Cytryn, E. Impact of anthropogenic activities on the dissemination of antibiotic resistance across ecological boundaries. Essays Biochem. 61, 11–21 (2017).

    PubMed  Article  Google Scholar 

  181. 181.

    Chantziaras, I., Boyen, F., Callens, B. & Dewulf, J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J. Antimicrob. Chemother. 69, 827–834 (2014).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

The authors acknowledge the collaborative nature of the work on the rumen microbiome by thanking the global scientific community involved in rumen microbiome research and the deciphering of its mysteries. The authors also thank E. Jami (Agricultural Research Organization, Volcani Center, Israel) and E. A. Bayer (The Weizmann Institute of Science, Israel) for critical reading of the manuscript. Research in the authors’ laboratory was supported by grants from the European Research Council (No. 640384) to I.M. and from the Israel Science Foundation (ISF No. 1947/19) to I.M. and S.M.

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I.M. and S.M. researched data for the article, substantially contributed to discussion of content and wrote the article. I.M., R.J.W. and S.M. conceptualized, reviewed and edited the manuscript before submission.

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Correspondence to Itzhak Mizrahi.

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Food and Agriculture Organization of the United Nations (FAOSTAT) enteric fermentation: http://www.fao.org/faostat/en/#data/GE

Glossary

Core microbiome

A group of microorganisms commonly found within the microbiome across multiple hosts.

Food webs

The interconnections among different microbial food chains.

Electron sinks

In this context, microorganisms within a microbial community that accept electrons at the final step of the electron flow.

Hydrogenotrophs

Methanogens that use H2 to reduce CO2 to methane.

Methylotrophs

Methanogens that use a methylated compound as the input metabolite to produce methane.

Acetoclastic methanogens

Methanogens that use acetate to produce methane.

Alternative stable community states

Assemblages of functional groups that are locked and stabilized by metabolic feedback and result in distinct composition, function and, thus, outcome.

Functional microbial groups

Groups of organisms that share similar functionality within the ecosystem.

Horizontal gene transfer

(HGT). The lateral mobilization of genetic material between distinct microorganisms.

Rumen plasmidome

The collective plasmid population in the rumen.

Resistome

The collection of antibiotic resistance genes in a given environment.

Biohydrogenation

The microbial transformation of unsaturated fatty acid to saturated fatty acid.

Residual feed intake

A parameter that describes feed efficiency, measuring the difference between the actual feed intake and the predicted intake, based on an animal’s body weight, weight gain and milk composition, and is a proxy for the animal’s ability to extract energy from its feed.

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Mizrahi, I., Wallace, R.J. & Moraïs, S. The rumen microbiome: balancing food security and environmental impacts. Nat Rev Microbiol (2021). https://doi.org/10.1038/s41579-021-00543-6

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