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Evolutionary Perspectives on the Human Gut Microbiome

Abstract

The renewed interest in human gut microbiome research spawned by modern developments in metagenomics resulted in many fascinating new results, but confusion and seeming contradictions are still common in this nascent field. As for other subdisciplines of biology, evolutionary biology serves as a unifying principle in studying host-microbe interactions. However, the range of perspectives offered by evolution is often not considered or fully appreciated in human gut microbiome research. In this chapter we provide a broad overview of evolutionary perspectives on the human gut microbiome, which range from the origin of holobionts to strain-level microbial variation within a host’s lifetime.

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References

  • Aiello, L. C., & Wheeler, P. (1995). The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution. Current Anthropology, 36, 199–221.

    CrossRef  Google Scholar 

  • Andrés, A. M., Hubisz, M. J., Indap, A., Torgerson, D. G., Degenhardt, J. D., Boyko, A. R., Gutenkunst, R. N., White, T. J., Green, E. D., Bustamante, C. D., et al. (2009). Targets of balancing selection in the human genome. Molecular Biology and Evolution, 26, 2755–2764.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Benson, A. K. (2015). Host genetic architecture and the landscape of microbiome composition: Humans weigh in. Genome Biology, 16, 203.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Berna, F., Goldberg, P., Horwitz, L. K., Brink, J., Holt, S., Bamford, M., & Chazan, M. (2012). Microstratigraphic evidence of in situ fire in the Acheulean strata of Wonderwerk Cave, Northern Cape province, South Africa. Proceedings of the National Academy of Sciences, 109, E1215–E1220.

    CrossRef  Google Scholar 

  • Blekhman, R., Goodrich, J. K., Huang, K., Sun, Q., Bukowski, R., Bell, J. T., Spector, T. D., Keinan, A., Ley, R. E., Gevers, D., et al. (2015). Host genetic variation impacts microbiome composition across human body sites. Genome Biology, 16, 191.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Bordenstein, S. R., & Theis, K. R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biology, 13, e1002226.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks, A. W., Kohl, K. D., Brucker, R. M., van Opstal, E. J., & Bordenstein, S. R. (2016). Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history. PLoS Biology, 14, e2000225.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Davenport, E. R., Goodrich, J. K., Bell, J. T., Spector, T. D., Ley, R. E., & Clark, A. G. (2016). ABO antigen and secretor statuses are not associated with gut microbiota composition in 1,500 twins. BMC Genomics, 17, 941.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • De Paepe, M., Gaboriau-Routhiau, V., Rainteau, D., Rakotobe, S., Taddei, F., & Cerf-Bensussan, N. (2011). Trade-off between bile resistance and nutritional competence drives Escherichia coli diversification in the mouse gut. PLoS Genetics, 7, e1002107.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobzhansky, T. (1973). Nothing in biology makes sense except in the light of evolution. The American Biology Teacher, 35(3), 125–129.

    CrossRef  Google Scholar 

  • Eisen, J. A. (2014, June). The tree of life: Microbiomania and “overselling the microbiome” [Blog post]. Retrieved from https://phylogenomics.blogspot.de/p/blog-page.html

  • Franzenburg, S., Fraune, S., Künzel, S., Baines, J. F., Domazet-Loso, T., & Bosch, T. C. G. (2012). MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers. Proceedings of the National Academy of Sciences of the United States of America, 109, 19374–19379.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Fumagalli, M., Cagliani, R., Pozzoli, U., Riva, S., Comi, G. P., Menozzi, G., Bresolin, N., & Sironi, M. (2009). Widespread balancing selection and pathogen-driven selection at blood group antigen genes. Genome Research, 19, 199–212.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillings, M. R., Paulsen, I. T., & Tetu, S. G. (2015). Ecology and evolution of the human microbiota: Fire, farming and antibiotics. Genes, 6, 841–857.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodrich, J. K., Davenport, E. R., Beaumont, M., Jackson, M. A., Knight, R., Ober, C., Spector, T. D., Bell, J. T., Clark, A. G., & Ley, R. E. (2016). Genetic determinants of the gut microbiome in UK twins. Cell Host & Microbe, 19, 731–743.

    CrossRef  CAS  Google Scholar 

  • Goodrich, J. K., Davenport, E. R., Clark, A. G., & Ley, R. E. (2017). The relationship between the human genome and microbiome comes into view. Annual Review of Genetics, 51, 413–433.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon, J., Knowlton, N., Relman, D. A., Rohwer, F., & Youle, M. (2013). Superorganisms and holobionts. Microbe Magazine, 8, 152–153.

    CrossRef  Google Scholar 

  • 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.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall, A. B., Tolonen, A. C., & Xavier, R. J. (2017). Human genetic variation and the gut microbiome in disease. Nature Reviews Genetics, 18, 690.

    CrossRef  CAS  PubMed  Google Scholar 

  • Karkanas, P., Shahackgross, R., Ayalon, A., Barmatthews, M., Barkai, R., Frumkin, A., Gopher, A., & Stiner, M. (2007). Evidence for habitual use of fire at the end of the Lower Paleolithic: Site-formation processes at Qesem Cave, Israel. Journal of Human Evolution, 53, 197–212.

    CrossRef  PubMed  Google Scholar 

  • Ley, R. E., Peterson, D. A., & Gordon, J. I. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell, 124, 837–848.

    CrossRef  CAS  PubMed  Google Scholar 

  • Ley, R. E., Hamady, M., Lozupone, C., Turnbaugh, P. J., Ramey, R. R., Bircher, J. S., Schlegel, M. L., Tucker, T. A., Schrenzel, M. D., Knight, R., et al. (2008a). Evolution of mammals and their gut microbes. Science, 320, 1647–1651.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Ley, R. E., Lozupone, C. A., Hamady, M., Knight, R., & Gordon, J. I. (2008b). Worlds within worlds: Evolution of the vertebrate gut microbiota. Nature Reviews Microbiology, 6, 776–788.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Linnenbrink, M., Wang, J., Hardouin, E. A., Künzel, S., Metzler, D., & Baines, J. F. (2013). The role of biogeography in shaping diversity of the intestinal microbiota in house mice. Molecular Ecology, 22, 1904–1916.

    CrossRef  PubMed  Google Scholar 

  • Margulis, L. (1993). Symbiosis in cell evolution: Microbial communities in the Archean and Proterozoic eons. New York: Freeman.

    Google Scholar 

  • Margulis, L., & Fester, R. (Eds.). (1991). Symbiosis as a source of evolutionary innovation: Speciation and morphogenesis. Cambridge, MA: MIT Press.

    Google Scholar 

  • McFall-Ngai, M., Hadfield, M. G., Bosch, T. C. G., Carey, H. V., Domazet-Lošo, T., Douglas, A. E., Dubilier, N., Eberl, G., Fukami, T., Gilbert, S. F., et al. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229–3236.

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Moeller, A. H. (2017). The shrinking human gut microbiome. Current Opinion in Microbiology, 38, 30–35.

    CrossRef  CAS  PubMed  Google Scholar 

  • Moeller, A. H., Degnan, P. H., Pusey, A. E., Wilson, M. L., Hahn, B. H., & Ochman, H. (2012). Chimpanzees and humans harbour compositionally similar gut enterotypes. Nature Communications, 3, 1179.

    CrossRef  CAS  PubMed  Google Scholar 

  • Moeller, A. H., Li, Y., Mpoudi Ngole, E., Ahuka-Mundeke, S., Lonsdorf, E. V., Pusey, A. E., Peeters, M., Hahn, B. H., & Ochman, H. (2014). Rapid changes in the gut microbiome during human evolution. Proceedings of the National Academy of Sciences, 111, 16431–16435.

    CrossRef  CAS  Google Scholar 

  • Moeller, A. H., Caro-Quintero, A., Mjungu, D., Georgiev, A. V., Lonsdorf, E. V., Muller, M. N., Pusey, A. E., Peeters, M., Hahn, B. H., & Ochman, H. (2016). Cospeciation of gut microbiota with hominids. Science, 353, 380–382.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran, N. A., & Sloan, D. B. (2015). The hologenome concept: Helpful or hollow? PLoS Biology, 13, e1002311.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Perry, G. H., Dominy, N. J., Claw, K. G., Lee, A. S., Fiegler, H., Redon, R., Werner, J., Villanea, F. A., Mountain, J. L., Misra, R., et al. (2007). Diet and the evolution of human amylase gene copy number variation. Nature Genetics, 39, 1256–1260.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Rausch, P., Rehman, A., Kunzel, S., Hasler, R., Ott, S. J., Schreiber, S., Rosenstiel, P., Franke, A., & Baines, J. F. (2011). Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proceedings of the National Academy of Sciences, 108, 19030–19035.

    CrossRef  Google Scholar 

  • Richards, M. P. (2002). A brief review of the archaeological evidence for Palaeolithic and Neolithic subsistence. European Journal of Clinical Nutrition, 56, 16 p following 1262.

    Google Scholar 

  • Schnorr, S. L., Candela, M., Rampelli, S., Centanni, M., Consolandi, C., Basaglia, G., Turroni, S., Biagi, E., Peano, C., Severgnini, M., et al. (2014). Gut microbiome of the Hadza hunter-gatherers. Nature Communications, 5, 3654.

    CrossRef  CAS  PubMed  Google Scholar 

  • Shimelmitz, R., Kuhn, S. L., Jelinek, A. J., Ronen, A., Clark, A. E., & Weinstein-Evron, M. (2014). “Fire at will”: The emergence of habitual fire use 350,000 years ago. Journal of Human Evolution, 77, 196–203.

    CrossRef  PubMed  Google Scholar 

  • Singh, R. K., Chang, H.-W., Yan, D., Lee, K. M., Ucmak, D., Wong, K., Abrouk, M., Farahnik, B., Nakamura, M., Zhu, T. H., et al. (2017). Influence of diet on the gut microbiome and implications for human health. Journal of Translational Medicine, 15, 73.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Spor, A., Koren, O., & Ley, R. (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Reviews Microbiology, 9, 279–290.

    CrossRef  CAS  PubMed  Google Scholar 

  • Stevens, C. E., & Hume, I. D. (2004). Comparative physiology of the vertebrate digestive system. New York: Cambridge University Press.

    Google Scholar 

  • Theis, K. R., Dheilly, N. M., Klassen, J. L., Brucker, R. M., Baines, J. F., Bosch, T. C. G., Cryan, J. F., Gilbert, S. F., Goodnight, C. J., Lloyd, E. A., et al. (2016). Getting the hologenome concept right: An eco-evolutionary framework for hosts and their microbiomes. MSystems, 1, e00028–16.

    Google Scholar 

  • Tong, M., McHardy, I., Ruegger, P., Goudarzi, M., Kashyap, P. C., Haritunians, T., Li, X., Graeber, T. G., Schwager, E., Huttenhower, C., et al. (2014). Reprograming of gut microbiome energy metabolism by the FUT2 Crohn’s disease risk polymorphism. The ISME Journal, 8, 2193–2206.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009). A core gut microbiome in obese and lean twins. Nature, 457, 480–484.

    CrossRef  CAS  PubMed  Google Scholar 

  • Varki, A. (2006). Nothing in glycobiology makes sense, except in the light of evolution. Cell, 126, 841–845.

    CrossRef  CAS  PubMed  Google Scholar 

  • Walter, J., & Ley, R. (2011). The human gut microbiome: Ecology and recent evolutionary changes. Annual Review of Microbiology, 65, 411–429.

    CrossRef  CAS  PubMed  Google Scholar 

  • Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 5261–5267.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Thingholm, L. B., Skiecevičienė, J., Rausch, P., Kummen, M., Hov, J. R., Degenhardt, F., Heinsen, F.-A., Rühlemann, M. C., Szymczak, S., et al. (2016). Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nature Genetics, 48, 1396–1406.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Woese, C. R., & Fox, G. E. (1977). Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proceedings of the National Academy of Sciences of the United States of America, 74, 5088–5090.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, G. D., Chen, J., Hoffmann, C., Bittinger, K., Chen, Y.-Y., Keilbaugh, S. A., Bewtra, M., Knights, D., Walters, W. A., Knight, R., et al. (2011). Linking long-term dietary patterns with gut microbial enterotypes. Science, 334, 105–108.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsunenko, T., Rey, F. E., Manary, M. J., Trehan, I., Dominguez-Bello, M. G., Contreras, M., Magris, M., Hidalgo, G., Baldassano, R. N., Anokhin, A. P., et al. (2012). Human gut microbiome viewed across age and geography. Nature, 486, 222–227.

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, S., Lieberman, T. D., Poyet, M., Groussin, M., Gibbons, S. M., Xavier, R. J., & Alm, E. J. (2017). Adaptive evolution within the gut microbiome of individual people. BioRxiv. https://doi.org/10.1101/208009 [Preprint] March 9, 2018.

  • Zilber-Rosenberg, I., & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiology Reviews, 32, 723–735.

    CrossRef  CAS  PubMed  Google Scholar 

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Doms, S., Hermes, BM., Baines, J.F. (2018). Evolutionary Perspectives on the Human Gut Microbiome. In: Haller, D. (eds) The Gut Microbiome in Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-319-90545-7_5

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