Rates of gut microbiome divergence in mammals
Corresponding Author
Alex H. Nishida
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA
Correspondence
Alex H. Nishida, Department of Integrative Biology, University of Texas, Austin, TX, USA.
Email: [email protected]
Search for more papers by this authorHoward Ochman
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA
Search for more papers by this authorCorresponding Author
Alex H. Nishida
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA
Correspondence
Alex H. Nishida, Department of Integrative Biology, University of Texas, Austin, TX, USA.
Email: [email protected]
Search for more papers by this authorHoward Ochman
Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA
Search for more papers by this authorAbstract
The variation and taxonomic diversity among mammalian gut microbiomes raises several questions about the factors that contribute to the rates and patterns of change in these microbial communities. By comparing the microbiome compositions of 112 species representing 14 mammalian orders, we assessed how host and ecological factors contribute to microbiome diversification. Except in rare cases, the same bacterial phyla predominate in mammalian gut microbiomes, and there has been some convergence of microbiome compositions according to dietary category across all mammalians lineages except Chiropterans (bats), which possess high proportions of Proteobacteria and tend to be most similar to one another regardless of diet. At lower taxonomic ranks (families, genera, 97% OTUs), bacteria are more likely to be associated with a particular mammalian lineage than with a particular dietary category, resulting in a strong phylogenetic signal in the degree to which microbiomes diverge. Despite different physiologies, the gut microbiomes of several mammalian lineages have diverged at roughly the same rate over the past 75 million years; however, the gut microbiomes of Cetartiodactyla (ruminants, whales, hippopotami) have evolved much faster and those of Chiropterans much slower. Contrary to expectations, the number of dietary transitions within a lineage does not influence rates of microbiome divergence, but instead, some of the most dramatic changes are associated with the loss of bacterial taxa, such as those accompanying the transition from terrestrial to marine lifestyles and the evolution of hominids.
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REFERENCES
- Amato, K. R., Leigh, S. R., Kent, A., Mackie, R. I., Yeoman, C. J., Stumpf, R. M., & Garber, P. A. (2014). The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra). American Journal of Physical Anthropology, 155, 652–664. https://doi.org/10.1002/ajpa.22621
- Amato, K. R., Yeoman, C. J., Cerda, G., Danzy Cramer, J., Berg Miller, M. E., Gomez, A., & Leigh, S. R. (2015). Variable responses of human and non-human primate gut microbiomes to a Western diet. Microbiome, 3, 53. https://doi.org/10.1186/s40168-015-0120-7
- Andrews, S. (2010). fastqc: a quality control tool for high throughput sequence data. Retrieved from https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
- Blaser, M. J., & Falkow, S. (2009). What are the consequences of the disappearing human microbiota? Nature Reviews Microbiology, 7, 887–894. https://doi.org/10.1038/nrmicro2245
- Blekhman, R., Goodrich, J. K., Huang, K., Sun, Q., Bukowski, R., Bell, J. T., & Clark, A. G. (2015). Host genetic variation impacts microbiome composition across human body sites. Genome Biology, 16, 191. https://doi.org/10.1186/s13059-015-0759-1
- Bonder, M. J., Kurilshikov, A., Tigchelaar, E. F., Mujagic, Z., Imhann, F., Vila, A. V., & Zhernakova, D. V. (2016). The effect of host genetics on the gut microbiome. Nature Genetics, 48, 1407–1412. https://doi.org/10.1038/ng.3663
- Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., & Knight, R. (2010). qiime allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335–336. https://doi.org/10.1038/nmeth.f.303
- Carmody, R. N., Gerber, G. K., Luevano, J. M., Gatti, D. M., Somes, L., Svenson, K. L., & Turnbaugh, P. J. (2015). Diet dominates host genotype in shaping the murine gut microbiota. Cell Host and Microbe, 17, 72–84. https://doi.org/10.1016/j.chom.2014.11.010
- Carrillo-Araujo, M., Taş, N., Alcántara-Hernández, R. J., Gaona, O., Schondube, J. E., Medellín, R. A., & Falcón, L. I. (2015). Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies. Frontiers in Microbiology, 6, 447.
- Caviedes-Vidal, E., McWhorter, T. J., Lavin, S. R., Chediack, J. G., Tracy, C. R., Karasov, W. H. (2007). The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proceedings of the National Academy of Sciences, 104, 19132–19137.
- Clauss, M., Steuer, P., Müller, D. W. H., Codron, D., & Hummel, J. (2013). Herbivory and body size: Allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS One, 8, e68714. https://doi.org/10.1371/journal.pone.0068714
- Clayton, J. B., Vangay, P., Huang, H., Ward, T., Hillmann, B. M., Al-Ghalith, G. A., & Knights, D. (2016). Captivity humanizes the primate microbiome. Proceedings of the National Academy of Sciences of the United States of America, 113, 10376–10381. https://doi.org/10.1073/pnas.1521835113
- Clutton-Brock, T. H. (1991). The evolution of parental care. Princeton, NJ: Princeton University Press.
10.1515/9780691206981 Google Scholar
- Davenport, E. R., Cusanovich, D. A., Michelini, K., Barreiro, L. B., Ober, C., & Gilad, Y. (2015). Genome-wide association studies of the human gut microbiota. PLoS One, 10, e0140301. https://doi.org/10.1371/journal.pone.0140301
- Davenport, E. R., Mizrahi-Man, O., Michelini, K., Barreiro, L. B., Ober, C., & Gilad, Y. (2014). Seasonal variation in human gut microbiome composition. PLoS One, 9, e90731. https://doi.org/10.1371/journal.pone.0090731
- David, L. A., Maurice, C. F., Carmody, R. N., Gootenberg, D. B., Button, J. E., Wolfe, B. E., & Biddinger, S. B. (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature, 505, 559–563. https://doi.org/10.1038/nature12820
- De Filippo, C., Cavalieri, D., Di Paola, M., Ramazzotti, M., Poullet, J. B., Massart, S., & Lionetti, P. (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proceedings of the National Academy of Sciences of the United States of America, 107, 14691–14696. https://doi.org/10.1073/pnas.1005963107
- Degnan, P. H., Pusey, A. E., Lonsdorf, E. V., Goodall, J., Wroblewski, E. E., Wilson, M. L., & Ochman, H. (2012). Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences of the United States of America, 109, 13034–13039. https://doi.org/10.1073/pnas.1110994109
- Delsuc, F., Metcalf, J. L., Wegener Parfrey, L., Song, S. J., González, A., & Knight, R. (2014). Convergence of gut microbiomes in myrmecophagous mammals. Molecular Ecology, 23, 1301–1317. https://doi.org/10.1111/mec.12501
- Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., & Knight, R. (2011). uchime improves sensitivity and speed of chimera detection. Bioinformatics, 27, 2194–2200. https://doi.org/10.1093/bioinformatics/btr381
- Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biological Conservation, 61, 1–10. https://doi.org/10.1016/0006-3207(92)91201-3
- Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125, 1–15. https://doi.org/10.1086/284325
- Gilbert, J. A., Quinn, R. A., Debelius, J., Xu, Z. Z., Morton, J., Garg, N., & Knight, R. (2016). Microbiome-wide association studies link dynamic microbial consortia to disease. Nature, 535, 94–103. https://doi.org/10.1038/nature18850
- Gloor, G. B., Wu, J. R., Pawlowsky-Glahn, V., & Egozcue, J. J. (2016). It's all relative: Analyzing microbiome data as compositions. Annals of Epidemiology, 26, 322–329. https://doi.org/10.1016/j.annepidem.2016.03.003
- Godon, J. J., Arulazhagan, P., Steyer, J. P., & Hamelin, J. (2016). Vertebrate bacterial gut diversity: Size also matters. BMC Ecology, 16, 12. https://doi.org/10.1186/s12898-016-0071-2
- Gomez, A., Rothman, J. M., Petrzelkova, K., Yeoman, C. J., Vlckova, K., Umaña, J. D., & Leigh, S. R. (2016). Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp. The ISME Journal, 10, 514–526. https://doi.org/10.1038/ismej.2015.146
- Goodrich, J. K., Davenport, E. R., Beaumont, M., Jackson, M. A., Knight, R., Ober, C., & Ley, R. E. (2016). Genetic determinants of the gut microbiome in UK twins. Cell Host and Microbe, 19, 731–743. https://doi.org/10.1016/j.chom.2016.04.017
- Goodrich, J. K., Waters, J. L., Poole, A. C., Sutter, J. L., Koren, O., Blekhman, R., & Spector, T. D. (2014). Human genetics shape the gut microbiome. Cell, 159, 789–799. https://doi.org/10.1016/j.cell.2014.09.053
- Groussin, M., Mazel, F., Sanders, J. G., Smillie, C. S., Lavergne, S., Thuiller, W., & Alm, E. J. (2017). Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nature Communications, 8, 14319. https://doi.org/10.1038/ncomms14319
- Hale, V. L., Tan, C. L., Niu, K., Yang, Y., Knight, R., Zhang, Q., … Amato, K. R. (2018). Diet versus phylogeny: A comparison of gut microbiota in captive colobine monkey species. Microbial Ecology, 75, 515–527.
- Hird, S. M., Sánchez, C., Carstens, B. C., & Brumfield, R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. Frontiers in Microbiology, 6, 1403.
- Karasov, W. H., & Douglas, A. E. (2013). Comparative digestive physiology. Comprehensive Physiology, 3, 741–783.
- Kohl, K. D., & Dearing, M. D. (2014). Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environmental Microbiology Reports, 6, 191–195. https://doi.org/10.1111/1758-2229.12118
- Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., & Gordon, J. I. (2008). Evolution of mammals and their gut microbes. Science, 320, 1647–1651. https://doi.org/10.1126/science.1155725
- McKenzie, V. J., Song, S. J., Delsuc, F., Prest, T. L., Oliverio, A. M., Korpita, T. M., & Knight, R. (2017). The effects of captivity on the mammalian gut microbiome. Integrative and Comparative Biology, 486, 222–227.
- Moeller, A. H. A., Foerster, S., Wilson, M. L., Pusey, A. E., Hahn, B. H., & Ochman, H. (2016). Social behavior shapes the chimpanzee pan-microbiome. Science Advances, 2, e1500997. https://doi.org/10.1126/sciadv.1500997
- Moeller, A. H., Li, Y., Mpoudi Ngole, E., Ahuka-Mundeke, S., Lonsdorf, E. V., Pusey, A. E., & Ochman, H. (2014). Rapid changes in the gut microbiome during human evolution. Proceedings of the National Academy of Sciences of the United States of America, 111, 16431–16435. https://doi.org/10.1073/pnas.1419136111
- Moeller, A. H., Peeters, M., Ndjango, J.-B., Li, Y., Hahn, B. H., & Ochman, H. (2013). Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Research, 23, 1715–1720. https://doi.org/10.1101/gr.154773.113
- Morton, E. R., Lynch, J., Froment, A., Lafosse, S., Heyer, E., Przeworski, M., & Ségurel, L. (2015). Variation in rural African gut microbiota is strongly correlated with colonization by entamoeba and subsistence. PLoS Genetics, 11, e1005658. https://doi.org/10.1371/journal.pgen.1005658
- Muegge, B. D., Kuczynski, J., Knights, D., Clemente, J. C., González, A., Fontana, L., & Gordon, J. I. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science, 332, 970–974. https://doi.org/10.1126/science.1198719
- Nelson, T. M., Rogers, T. L., Carlini, A. R., & Brown, M. V. (2013). Diet and phylogeny shape the gut microbiota of Antarctic seals: A comparison of wild and captive animals. Environmental Microbiology, 15, 1132–1145. https://doi.org/10.1111/1462-2920.12022
- Nemergut, D. R., Schmidt, S. K., Fukami, T., O'Neill, S. P., Bilinski, T. M., Stanish, L. F., & Ferrenberg, S. (2013). Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews, 77, 342–356. https://doi.org/10.1128/MMBR.00051-12
- Ochman, H., Worobey, M., Kuo, C.-H., Ndjango, J.-B. N., Peeters, M., Hahn, B. H., & Hugenholtz, P. (2010). Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8, e1000546.
- O'Keefe, S. J. D., Li, J. V., Lahti, L., Ou, J., Carbonero, F., Mohammed, K., & Vipperla, K. (2015). Fat, fibre and cancer risk in African Americans and rural Africans. Nature Communications, 6, 6342. https://doi.org/10.1038/ncomms7342
- Phillips, C. D., Phelan, G., Dowd, S. E., McDonuough, M. M., Ferguson, A. W., Delton Hanson, J., & Baker, R. J. (2012). Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. Molecular Ecology, 21, 2617–2627. https://doi.org/10.1111/j.1365-294X.2012.05568.x
- Porter, L. M., Sterr, S. M., & Garber, P. A. (2007). Habitat use and ranging behavior of Callimico goeldii. International Journal of Primatology, 28, 1035–1058. https://doi.org/10.1007/s10764-007-9205-x
- Price, E. R., Brun, A., Caviedes-Vidal, E., & Karasov, W. H. (2015). Digestive adaptations of aerial lifestyles. Physiology, 30, 69–78. https://doi.org/10.1152/physiol.00020.2014
- Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., & Glöckner, F. O. (2012). The silva ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590–D596. https://doi.org/10.1093/nar/gks1219
- Rampelli, S., Schnorr, S. L., Consolandi, C., Turroni, S., Severgnini, M., Peano, C., & Candela, M. (2015). Metagenome sequencing of the Hadza hunter-gatherer gut microbiota. Current Biology, 25, 1682–1693. https://doi.org/10.1016/j.cub.2015.04.055
- Roggenbuck, M., Schnell, I. B., Blom, N., Bælum, J., Bertelsen, M. F., Sicheritz-Pontén, T., & Hansen, L. H. (2014). The microbiome of New World vultures. Nature Communications, 5, 5498. https://doi.org/10.1038/ncomms6498
- Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahé, F. (2016). vsearch: A versatile open source tool for metagenomics. PeerJ, 4, e2584. https://doi.org/10.7717/peerj.2584
- Sanders, J. G., Beichman, A. C., Roman, J., Scott, J. J., Emerson, D., McCarthy, J. J., & Girguis, P. R. (2015). Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nature Communications, 6, 8285. https://doi.org/10.1038/ncomms9285
- Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., & Sahl, J. W. (2009). Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541. https://doi.org/10.1128/AEM.01541-09
- Schmieder, R., & Edwards, R. (2011). Quality control and preprocessing of metagenomic datasets. Bioinformatics, 27, 863–864. https://doi.org/10.1093/bioinformatics/btr026
- Song, S. J., Lauber, C., Costello, E. K., Lozupone, C. A., Humphrey, G., Berg-Lyons, D., … Gordon, J. I. (2013). Cohabiting family members share microbiota with one another and with their dogs. eLife, 2, e00458.
- Storey, A. E., & Ziegler, T. E. (2016). Primate paternal care: Interactions between biology and social experience. Hormones and Behavior, 77, 260–271. https://doi.org/10.1016/j.yhbeh.2015.07.024
- Sun, B., Wang, X., Bernstein, S., Huffman, M. A., Xia, D.-P., Gu, Z., & Li, J. (2016). Marked variation between winter and spring gut microbiota in free-ranging Tibetan Macaques (Macaca thibetana). Scientific Reports, 6, 26035. https://doi.org/10.1038/srep26035
- Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J.-C., Lynch, J., Grieneisen, L. E., … Archie, E. A. (2015). Social networks predict gut microbiome composition in wild baboons. eLife, 4, e05224.
- Turnbaugh, P. J., Ridaura, V. K., Faith, J. J., Rey, F. E., Knight, R., & Gordon, J. I. (2009). The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine, 1, 6ra14.
- Weiss, S., Xu, Z. Z., Peddada, S., Amir, A., Bittinger, K., Gonzalez, A., Hyde, E. R. (2017). Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome, 5, 27. https://doi.org/10.1186/s40168-017-0237-y
- Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., & Lewis, J. D. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science, 334, 105–108. https://doi.org/10.1126/science.1208344
- Xue, Z., Zhang, W., Wang, L., Hou, R., Zhang, M., Fei, L., … Zhang, Z. (2015). The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. mBio, 6, 1–12.
- Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., & Gordon, J. I. (2012). Human gut microbiome viewed across age and geography. Nature, 486, 222–227.
- Yuan, S., Cohen, D. B., Ravel, J., Abdo, Z., & Forney, L. J. (2012). Evaluation of methods for the extraction and purification of DNA from the human microbiome. PLoS One, 7, e33865. https://doi.org/10.1371/journal.pone.0033865
- Zhu, L., Wu, Q., Dai, J., Zhang, S., & Wei, F. (2011). Evidence of cellulose metabolism by the giant panda gut microbiome. Proceedings of the National Academy of Sciences of the United States of America, 108, 17714–17719. https://doi.org/10.1073/pnas.1017956108
Citing Literature
Special Issue:THE HOST‐ASSOCIATED MICROBIOME: PATTERN, PROCESS AND FUNCTION
April 2018
Pages 1884-1897