A catalog of microbial genes from the bovine rumen unveils a specialized and diverse biomass-degrading environment

  1. Junhua Li
  2. Huanzi Zhong
  3. Yuliaxis Ramayo-Caldas
  4. Nicolas Terrapon
  5. Vincent Lombard
  6. Gabrielle Potocki-Veronese
  7. Jordi Estellé
  8. Milka Popova
  9. Ziyi Yang
  10. Hui Zhang
  11. Fang Li
  12. Shanmei Tang
  13. Fangming Yang
  14. Weineng Chen
  15. Bing Chen
  16. Jiyang Li
  17. Jing Guo
  18. Cécile Martin
  19. Emmanuelle Maguin
  20. Xun Xu
  21. Huanming Yang
  22. Jian Wang
  23. Lise Madsen
  24. Karsten Kristiansen
  25. Bernard Henrissat
  26. Stanislav D Ehrlich
  27. Diego P Morgavi

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Abstract

Background

The rumen microbiota provides essential services to its host and, through its role in ruminant production, contributes to human nutrition and food security. A thorough knowledge of the genetic potential of rumen microbes will provide opportunities for improving the sustainability of ruminant production systems. The availability of gene reference catalogs from gut microbiomes has advanced the understanding of the role of the microbiota in health and disease in humans and other mammals. In this work, we established a catalog of reference prokaryote genes from the bovine rumen.

Results

Using deep metagenome sequencing we identified 13,825,880 non-redundant prokaryote genes from the bovine rumen. Compared to human, pig, and mouse gut metagenome catalogs, the rumen is larger and richer in functions and microbial species associated with the degradation of plant cell wall material and production of methane. Genes encoding enzymes catalyzing the breakdown of plant polysaccharides showed a particularly high richness that is otherwise impossible to infer from available genomes or shallow metagenomics sequencing. The catalog expands the dataset of carbohydrate-degrading enzymes described in the rumen. Using an independent dataset from a group of 77 cattle fed 4 common dietary regimes, we found that only <0.1% of genes were shared by all animals, which contrast with a large overlap for functions, i.e., 63% for KEGG functions. Different diets induced differences in the relative abundance rather than the presence or absence of genes, which explains the great adaptability of cattle to rapidly adjust to dietary changes.

Conclusions

These data bring new insights into functions, carbohydrate-degrading enzymes, and microbes of the rumen to complement the available information on microbial genomes. The catalog is a significant biological resource enabling deeper understanding of phenotypes and biological processes and will be expanded as new data are made available.

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  1. GigaScience

    Now published in GigaScience doi: 10.1093/gigascience/giaa057

    Junhua Li 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, China3School of Bioscience & Bioengineering, South China University of Technology, Guangzhou, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteORCID record for Junhua LiHuanzi Zhong 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteORCID record for Huanzi ZhongYuliaxis Ramayo-Caldas 4INRA, Institut National de la Recherche Agronomique, Génétique Animale et Biologie Intégrative, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, France5Animal Breeding and Genetics Program, Institute for Research and Technology in Food and Agriculture (IRTA), Torre Marimon, Caldes de Montbui, 08140, SpainFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteNicolas Terrapon 6CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France7INRA, USC 1408 AFMB, 13288 Marseille, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteVincent Lombard 6CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France7INRA, USC 1408 AFMB, 13288 Marseille, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteGabrielle Potocki-Veronese 8LISBP, Universite de Toulouse, CNRS, INRA, INSA, 31077, Toulouse, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteJordi Estellé 4INRA, Institut National de la Recherche Agronomique, Génétique Animale et Biologie Intégrative, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteMilka Popova 9INRA, UMR Herbivores, Université Clermont Auvergne, VetAgro Sup, F-63122 Saint-Genès Champanelle, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteZiyi Yang 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteHui Zhang 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteFang Li 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteShanmei Tang 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteWeineng Chen 1BGI-Shenzhen, Shenzhen 518083, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteBing Chen 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteJiyang Li 1BGI-Shenzhen, Shenzhen 518083, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteJing Guo 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteCécile Martin 9INRA, UMR Herbivores, Université Clermont Auvergne, VetAgro Sup, F-63122 Saint-Genès Champanelle, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteEmmanuelle Maguin 10INRA, Micalis Institute, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteXun Xu 1BGI-Shenzhen, Shenzhen 518083, China2China National GeneBank, BGI-Shenzhen, Shenzhen 518120, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteHuanming Yang 1BGI-Shenzhen, Shenzhen 518083, China11James D. Watson Institute of Genome Sciences, Hangzhou 310058, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteJian Wang 1BGI-Shenzhen, Shenzhen 518083, China11James D. Watson Institute of Genome Sciences, Hangzhou 310058, ChinaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteLise Madsen 1BGI-Shenzhen, Shenzhen 518083, China12Institute of Marine Research (IMR), Postboks 1870 Nordnes, 5817 Bergen, Norway13Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, 2100 Copenhagen Ø, DenmarkFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteKarsten Kristiansen 1BGI-Shenzhen, Shenzhen 518083, China13Laboratory of Genomics and Molecular Biomedicine, Department of Biology, University of Copenhagen, 2100 Copenhagen Ø, DenmarkFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteFor correspondence: diego.morgavi@inra.fr stanislav.ehrlich@inra.fr kk@bio.ku.dkBernard Henrissat 6CNRS UMR 7257, Aix-Marseille University, 13288 Marseille, France7INRA, USC 1408 AFMB, 13288 Marseille, France14Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi ArabiaFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteStanislav D. Ehrlich 15MGP MetaGenoPolis, INRA, Université Paris-Saclay, 78350 Jouy en Josas, France16Centre for Host Microbiome Interactions, Dental Institute, King’s College London, UKFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteFor correspondence: diego.morgavi@inra.fr stanislav.ehrlich@inra.fr kk@bio.ku.dkDiego P. Morgavi 9INRA, UMR Herbivores, Université Clermont Auvergne, VetAgro Sup, F-63122 Saint-Genès Champanelle, FranceFind this author on Google ScholarFind this author on PubMedSearch for this author on this siteORCID record for Diego P. MorgaviFor correspondence: diego.morgavi@inra.fr stanislav.ehrlich@inra.fr kk@bio.ku.dk

    A version of this preprint has been published in the Open Access journal GigaScience (see paper https://doi.org/10.1093/gigascience/giaa057 ), where the paper and peer reviews are published openly under a CC-BY 4.0 license.

    These peer reviews were as follows:

    Reviewer 1: http://dx.doi.org/10.5524/REVIEW.102258 Reviewer 2: http://dx.doi.org/10.5524/REVIEW.102259

  2. Version published to 10.1093/gigascience/giaa057
  3. Version published to 10.1101/272690v2 on bioRxiv
  4. Version published to 10.1101/272690v1 on bioRxiv