Review Article | Published:

A great-ape view of the gut microbiome

Nature Reviews Geneticsvolume 20pages195206 (2019) | Download Citation


Humans assemble a specialized microbiome from a world teeming with diverse microorganisms. Comparison to the microbiomes of great apes provides a dimension that is indispensable to understanding how these microbial communities form, function and change. This evolutionary perspective exposes not only how human gut microbiomes have been shaped by our great-ape heritage but also the features that make humans unique, as exemplified by an expansive loss of bacterial and archaeal diversity and the identification of microbial lineages that have co-diversified with their hosts.

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  1. 1.

    Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).

  2. 2.

    Arrieta, M.-C. et al. The intestinal microbiome in early life: health and disease. Front. Immunol. 5, 427 (2014).

  3. 3.

    Levy, M., Kolodziejczyk, A. A., Thaiss, C. A. & Elinav, E. Dysbiosis and the immune system. Nat. Rev. Immunol. 17, 219–232 (2017).

  4. 4.

    Gilbert, J. A. et al. Current understanding of the human microbiome. Nat. Med. 24, 392–400 (2018).

  5. 5.

    Yadav, M., Verma, M. K. & Chauhan, N. S. A review of metabolic potential of human gut microbiome in human nutrition. Arch. Microbiol. 200, 203–217 (2018).

  6. 6.

    Sommer, F. & Bäckhed, F. The gut microbiota — masters of host development and physiology. Nat. Rev. Microbiol. 11, 227–238 (2013).

  7. 7.

    Iyer, S. S. & Blumberg, R. S. in Physiology of the Gastrointestinal Tract 6th edn (eds Said, H. M., Ghishan, F. K., Kaunitz, J. D., Merchant, J. L. & Wood, J. D.) 767–774 (Academic Press, 2018).

  8. 8.

    David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014). This report demonstrates that human individuals assigned to different dietary groups diverged in the compositions of their gut microbiomes.

  9. 9.

    Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).

  10. 10.

    Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016).

  11. 11.

    Schmidt, T. S. B., Raes, J. & Bork, P. The human gut microbiome: from association to modulation. Cell 172, 1198–1215 (2018).

  12. 12.

    Gibbons, S. M., Duvallet, C. & Alm, E. J. Correcting for batch effects in case-control microbiome studies. PLOS Comput. Biol. 14, e1006102 (2018).

  13. 13.

    Blaser, M. J. The theory of disappearing microbiota and the epidemics of chronic diseases. Nat. Rev. Immunol. 17, 461–463 (2017). This commentary posits that the reduction in microorganisms in contemporary human populations is responsible for increases in autoimmune, metabolic and neurological disorders.

  14. 14.

    Duvallet, C., Gibbons, S. M., Gurry, T., Irizarry, R. A. & Alm, E. J. Meta-analysis of gut microbiome studies identifies disease-specific and shared responses. Nat. Commun. 8, 1784 (2017).

  15. 15.

    De Filippo, C. et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691–14696 (2010). This pioneering study shows that dietary differences in African and European children were associated with differences in the composition of the gut microbiome.

  16. 16.

    Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 (2011).

  17. 17.

    Goodrich, J. K., Davenport, E. R., Clark, A. G. & Ley, R. E. The relationship between the human genome and microbiome comes into view. Annu. Rev. Genet. 51, 413–433 (2017).

  18. 18.

    Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012). This paper serves as the foundational survey of the variation of the human gut microbiome across populations.

  19. 19.

    Clemente, J. C. et al. The microbiome of uncontacted Amerindians. Sci. Adv. 1, e1500183 (2015).

  20. 20.

    Smits, S. A. et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 357, 802–805 (2017).

  21. 21.

    Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl Acad. Sci. USA 108, 4578–4585 (2011).

  22. 22.

    Maurice, C. F., Haiser, H. J. & Turnbaugh, P. J. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152, 39–50 (2014).

  23. 23.

    Debelius, J. et al. Tiny microbes, enormous impacts: what matters in gut microbiome studies? Genome Biol. 17, 217 (2016).

  24. 24.

    Kundu, P., Blacher, E., Elinav, E. & Pettersson, S. Our gut microbiome: the evolving inner self. Cell 171, 1481–1493 (2017).

  25. 25.

    Davenport, E. R. et al. The human microbiome in evolution. BMC Biol. 15, 127 (2017).

  26. 26.

    Sze, M. A. & Schloss, P. D. Looking for a signal in the noise: revisiting obesity and the microbiome. mBio 7, e01018-16 (2016). This analysis shows that many publications reporting an association between microbiome composition and obesity were baseless.

  27. 27.

    Blekhman, R. et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 16, 191 (2015).

  28. 28.

    Bonder, M. J. et al. The effect of host genetics on the gut microbiome. Nat. Genet. 48, 1407–1412 (2016).

  29. 29.

    Goodrich, J. K. et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731–743 (2016). This study identifies heritable members of the human microbiome and the genetic factors influencing the abundance of certain bacterial taxa.

  30. 30.

    Wang, J. et al. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat. Genet. 48, 1396–1406 (2016).

  31. 31.

    Wood, B. & Harrison, T. The evolutionary context of the first hominins. Nature 470, 347–352 (2011).

  32. 32.

    Langergraber, K. E. et al. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc. Natl Acad. Sci. USA 109, 15716–15721 (2012).

  33. 33.

    Kronenberg, Z. N. et al. High-resolution comparative analysis of great ape genomes. Science 360, eaar6343 (2018).

  34. 34.

    Weiss, A. et al. Personality in the chimpanzees of Gombe National Park. Sci. Data 4, 170146 (2017).

  35. 35.

    Pusey, A. E., Pintea, L., Wilson, M. L., Kamenya, S. & Goodall, J. The contribution of long-term research at Gombe National Park to chimpanzee conservation. Conserv. Biol. 21, 623–634 (2007).

  36. 36.

    Moeller, A. H. et al. SIV-induced instability of the chimpanzee gut microbiome. Cell Host Microbe 14, 340–345 (2013).

  37. 37.

    Barbian, H. J. et al. Destabilization of the gut microbiome marks the end-stage of simian immunodeficiency virus infection in wild chimpanzees. Am. J. Primatol. 80, e22515 (2018).

  38. 38.

    Moeller, A. H. et al. Rapid changes in the gut microbiome during human evolution. Proc. Natl Acad. Sci. USA 111, 16431–16435 (2014).

  39. 39.

    Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011).

  40. 40.

    Knights, D. et al. Rethinking enterotypes. Cell Host Microbe 16, 433–437 (2014).

  41. 41.

    Jeffery, I. B., Claesson, M. J., O’Toole, P. W. & Shanahan, F. Categorization of the gut microbiota: enterotypes or gradients? Nat. Rev. Microbiol. 10, 591–592 (2012).

  42. 42.

    Costea, P. I. et al. Enterotypes in the landscape of gut microbial community composition. Nat. Microbiol. 3, 8–16 (2017). This study is a comprehensive examination of the evidence concerning the existence of enterotypes.

  43. 43.

    Newton-Fisher, N. E. in Handbook of Paleoanthropology (eds Henke, W. & Tattersall, I.) 1295–1320 (Springer Berlin Heidelberg, 2007).

  44. 44.

    Moeller, A. H. et al. Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat. Commun. 3, 1179 (2012).

  45. 45.

    Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1786 (2018).

  46. 46.

    Ramayo-Caldas, Y. et al. Phylogenetic network analysis applied to pig gut microbiota identifies an ecosystem structure linked with growth traits. ISME J. 10, 2973–2977 (2016).

  47. 47.

    Wang, J. et al. Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc. Natl Acad. Sci. USA 111, E2703–E2710 (2014).

  48. 48.

    Blaser, M. J. & Falkow, S. What are the consequences of the disappearing human microbiota? Nat. Rev. Microbiol. 7, 887–894 (2009).

  49. 49.

    Prüfer, K. et al. The bonobo genome compared with the chimpanzee and human genomes. Nature 486, 527–531 (2012).

  50. 50.

    Scally, A. et al. Insights into hominid evolution from the gorilla genome sequence. Nature 483, 169–175 (2012).

  51. 51.

    Ochman, H. et al. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLOS Biol. 8, e1000546 (2010).

  52. 52.

    Degnan, P. H. et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc. Natl Acad. Sci. USA 109, 13034–13039 (2012).

  53. 53.

    Gomez, A. et al. Temporal variation selects for diet-microbe co-metabolic traits in the gut of Gorilla spp. ISME J. 10, 514–526 (2016).

  54. 54.

    Yildirim, S. et al. Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities. PLOS ONE 5, e13963 (2010).

  55. 55.

    Martínez, I. et al. The gut microbiota of rural Papua New Guineans: composition, diversity patterns, and ecological processes. Cell Rep. 11, 527–538 (2015).

  56. 56.

    Moeller, A. H. et al. Cospeciation of gut microbiota with hominids. Science 353, 380–382 (2016).

  57. 57.

    Toju, H., Tanabe, A. S., Notsu, Y., Sota, T. & Fukatsu, T. Diversification of endosymbiosis: replacements, co-speciation and promiscuity of bacteriocyte symbionts in weevils. ISME J. 7, 1378–1390 (2013).

  58. 58.

    Clark, M. A., Moran, N. A., Baumann, P. & Wernegreen, J. J. Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54, 517–525 (2000).

  59. 59.

    Moran, N. A. & Sloan, D. B. The hologenome concept: helpful or hollow? PLOS Biol. 13, e1002311 (2015). This article represents a critical assessment of a purportedly new paradigm.

  60. 60.

    Ochman, H., Elwyn, S. & Moran, N. A. Calibrating bacterial evolution. Proc. Natl Acad. Sci. USA 96, 12638–12643 (1999).

  61. 61.

    Moran, N. A., Munson, M. A., Baumann, P. & Ishikawa, H. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc. R. Soc. B 253, 167–171 (1993).

  62. 62.

    Brito, I. L. & Alm, E. J. Tracking strains in the microbiome: insights from metagenomics and models. Front. Microbiol. 7, 712 (2016).

  63. 63.

    Caro-Quintero, A. & Ochman, H. Assessing the unseen bacterial diversity in microbial communities. Genome Biol. Evol. 7, 3416–3425 (2015).

  64. 64.

    Martino, M. E. et al. Bacterial adaptation to the host’s diet is a key evolutionary force shaping Drosophila-Lactobacillus symbiosis. Cell Host Microbe 24, 109–119 (2018).

  65. 65.

    King, K. C. et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J. 10, 1915–1924 (2016).

  66. 66.

    Thaiss, C. A. et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159, 514–529 (2014).

  67. 67.

    Schnorr, S. L. et al. Gut microbiome of the Hadza hunter-gatherers. Nat. Commun. 5, 3654 (2014).

  68. 68.

    Obregon-Tito, A. J. et al. Subsistence strategies in traditional societies distinguish gut microbiomes. Nat. Commun. 6, 6505 (2015).

  69. 69.

    Segata, N. Gut microbiome: westernization and the disappearance of intestinal diversity. Curr. Biol. 25, R611–R613 (2015).

  70. 70.

    Raymann, K., Moeller, A. H., Goodman, A. L. & Ochman, H. Unexplored archaeal diversity in the great ape gut microbiome. mSphere 2, e00026-17 (2017).

  71. 71.

    Flahou, B. et al. Diversity of zoonotic enterohepatic Helicobacter species and detection of a putative novel gastric Helicobacter species in wild and wild-born captive chimpanzees and western lowland gorillas. Vet. Microbiol. 174, 186–194 (2014).

  72. 72.

    Clayton, J. B. et al. Captivity humanizes the primate microbiome. Proc. Natl Acad. Sci. USA 113, 10376–10381 (2016). This study recapitulates in captive apes the loss of microbiome diversity apparent in humans.

  73. 73.

    Sonnenburg, E. D. et al. Diet-induced extinctions in the gut microbiota compound over generations. Nature 529, 212–215 (2016). This study reports that descendants of mice fed a high-fat, simple-carbohydrate diet were unable to regain microbial diversity even after returning to a fibre-rich diet.

  74. 74.

    Korpela, K. et al. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 28, 561–568 (2018).

  75. 75.

    Yildirim, S. et al. Primate vaginal microbiomes exhibit species specificity without universal Lactobacillus dominance. ISME J. 8, 2431–2444 (2014).

  76. 76.

    Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133–145 (2018).

  77. 77.

    Yassour, M. et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe 24, 146–154 (2018). This study scrutinizes the prevalence and functions of the specific bacterial strains that infants acquire from their mothers.

  78. 78.

    Marcobal, A. et al. Bacteroides in the infant gut consume milk oligosaccharides via mucus-utilization pathways. Cell Host Microbe 10, 507–514 (2011).

  79. 79.

    Sela, D. A. & Mills, D. A. Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides. Trends Microbiol. 18, 298–307 (2010).

  80. 80.

    Song, S. J. et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2, e00458 (2013).

  81. 81.

    Meadow, J. F., Bateman, A. C., Herkert, K. M., O’Connor, T. K. & Green, J. L. Significant changes in the skin microbiome mediated by the sport of roller derby. PeerJ 1, e53 (2013).

  82. 82.

    Kort, R. et al. Shaping the oral microbiota through intimate kissing. Microbiome 2, 41 (2014).

  83. 83.

    Browne, H. P., Neville, B. A., Forster, S. C. & Lawley, T. D. Transmission of the gut microbiota: spreading of health. Nat. Rev. Microbiol. 15, 531–543 (2017).

  84. 84.

    Moeller, A. H. et al. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2, e1500997 (2016).

  85. 85.

    Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. eLife 4, e05224 (2015).

  86. 86.

    Mosites, E. et al. Microbiome sharing between children, livestock and household surfaces in western Kenya. PLOS ONE 12, e0171017 (2017).

  87. 87.

    Ellis, R. J. et al. Comparison of the distal gut microbiota from people and animals in Africa. PLOS ONE 8, e54783 (2013).

  88. 88.

    Moeller, A. H. et al. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 23, 1715–1720 (2013).

  89. 89.

    Mehta, R. S. et al. Stability of the human faecal microbiome in a cohort of adult men. Nat. Microbiol. 3, 347–355 (2018).

  90. 90.

    Lloyd-Price, J. et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature 550, 61–66 (2017).

  91. 91.

    Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).

  92. 92.

    Caporaso, J. G. et al. Moving pictures of the human microbiome. Genome Biol. 12, R50 (2011). This paper title is easily the best for a longitudinal survey of microbiomes.

  93. 93.

    Costello, E. K. et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 (2009).

  94. 94.

    Odamaki, T. et al. Age-related changes in gut microbiota composition from newborn to centenarian: a cross-sectional study. BMC Microbiol. 16, 90 (2016).

  95. 95.

    Saraswati, S. & Sitaraman, R. Aging and the human gut microbiota — from correlation to causality. Front. Microbiol. 5, 764 (2015).

  96. 96.

    Mueller, N. T., Bakacs, E., Combellick, J., Grigoryan, Z. & Dominguez-Bello, M. G. The infant microbiome development: mom matters. Trends Mol. Med. 21, 109–117 (2015).

  97. 97.

    Badescu, I., Katzenberg, M. A., Watts, D. P. & Sellen, D. W. A novel fecal stable isotope approach to determine the timing of age-related feeding transitions in wild infant chimpanzees. Am. J. Phys. Anthropol. 162, 285–299 (2017).

  98. 98.

    Arboleya, S., Watkins, C., Stanton, C. & Ross, R. P. Gut Bifidobacteria populations in human health and aging. Front. Microbiol. 7, 1204 (2016).

  99. 99.

    Mariat, D. et al. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiol. 9, 123 (2009).

  100. 100.

    Million, M. et al. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. Int. J. Obes. 37, 1460–1466 (2013).

  101. 101.

    Dridi, B., Henry, M., El Khéchine, A., Raoult, D. & Drancourt, M. High prevalence of Methanobrevibacter smithii and Methanosphaera stadtmanae detected in the human gut using an improved DNA detection protocol. PLOS ONE 4, e7063 (2009).

  102. 102.

    Eloe-Fadrosh, E. A., Ivanova, N. N., Woyke, T. & Kyrpides, N. C. Metagenomics uncovers gaps in amplicon-based detection of microbial diversity. Nat. Microbiol. 1, 15032 (2016).

  103. 103.

    Koskinen, K. et al. First insights into the diverse human archaeome: specific detection of archaea in the gastrointestinal tract, lung, and nose and on skin. mBio 8, e00824-17 (2017).

  104. 104.

    Morris, B. E. L., Henneberger, R., Huber, H. & Moissl-Eichinger, C. Microbial syntrophy: interaction for the common good. FEMS Microbiol. Rev. 37, 384–406 (2013).

  105. 105.

    Lovley, D. R. Happy together: microbial communities that hook up to swap electrons. ISME J. 11, 327–336 (2017).

  106. 106.

    Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425 (2010).

  107. 107.

    Sharp, P. M. et al. Source of the human malaria parasite Plasmodium falciparum. Proc. Natl Acad. Sci. USA 108, E744–E745 (2011).

  108. 108.

    Hirsch, V. M., Olmsted, R. A., Murphey-Corb, M., Purcell, R. H. & Johnson, P. R. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339, 389–392 (1989).

  109. 109.

    Sharp, P. M. & Hahn, B. H. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1, a006841 (2011).

  110. 110.

    D’arc, M. et al. Origin of the HIV-1 group O epidemic in western lowland gorillas. Proc. Natl Acad. Sci. USA 112, E1343–E1352 (2015).

  111. 111.

    Huet, T., Cheynier, R., Meyerhans, A., Roelants, G. & Wain-Hobson, S. Genetic organization of a chimpanzee lentivirus related to HIV-1. Nature 345, 356–359 (1990).

  112. 112.

    Gao, F. et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397, 436–441 (1999).

  113. 113.

    Duval, L. et al. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc. Natl Acad. Sci. USA 107, 10561–10566 (2010).

  114. 114.

    Liu, W. et al. Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species. Nat. Commun. 8, 1635 (2017).

  115. 115.

    Prugnolle, F. et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc. Natl Acad. Sci. USA 107, 1458–1463 (2010).

  116. 116.

    Liu, W. et al. African origin of the malaria parasite Plasmodium vivax. Nat. Commun. 5, 3346 (2014).

  117. 117.

    Leendertz, F. H. et al. Anthrax kills wild chimpanzees in a tropical rainforest. Nature 430, 451–452 (2004).

  118. 118.

    Köndgen, S. et al. Pandemic human viruses cause decline of endangered great apes. Curr. Biol. 18, 260–264 (2008).

  119. 119.

    Leroy, E. M. et al. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 303, 387–390 (2004).

  120. 120.

    Bermejo, M. et al. Ebola outbreak killed 5000 gorillas. Science 314, 1564 (2006).

  121. 121.

    Kaur, T. et al. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am. J. Primatol. 70, 755–765 (2008).

  122. 122.

    Rwego, I. B., Isabirye-Basuta, G., Gillespie, T. R. & Goldberg, T. L. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv. Biol. 22, 1600–1607 (2008).

  123. 123.

    Nguyen, N., Warnow, T., Pop, M. & White, B. A perspective on 16S rRNA operational taxonomic unit clustering using sequence similarity. NPJ Biofilms Microbiomes 2, 16004 (2016).

  124. 124.

    Cole, J. R. et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642 (2014).

  125. 125.

    DeSantis, T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006).

  126. 126.

    Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596 (2013).

  127. 127.

    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

  128. 128.

    Amir, A. et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, e00191-16 (2017).

  129. 129.

    Nayfach, S. & Pollard, K. S. Toward accurate and quantitative comparative metagenomics. Cell 166, 1103–1116 (2016).

  130. 130.

    Davenport, E. R. et al. Seasonal variation in human gut microbiome composition. PLOS ONE 9, e90731 (2014).

  131. 131.

    Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018). This report on a substantive cohort study of Israelis identifies the environmental factors that shape the composition of the gut microbiome.

  132. 132.

    Jašarevic, E., Morrison, K. E. & Bale, T. L. Sex differences in the gut microbiome-brain axis across the lifespan. Phil. Trans. R. Soc. B 371, 20150122 (2016).

  133. 133.

    Barbian, H. J. et al. Neutralization properties of simian immunodeficiency viruses infecting chimpanzees and gorillas. mBio 6, e00296-15 (2015).

  134. 134.

    Williams, B., Landay, A. & Presti, R. M. Microbiome alterations in HIV infection a review. Cell. Microbiol. 18, 645–651 (2016).

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The authors thank K. Hammond for assistance with preparation of the figures. This work was supported by grants from the US National Institutes of Health (R35 GM118038 to H.O.) and the US National Science Foundation (Graduate Research Fellowship 2016226761 to A.H.N.).

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  1. Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA

    • Alex H. Nishida
    •  & Howard Ochman


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The authors contributed equally to all aspects of this manuscript.

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The authors declare no competing interests.

Corresponding author

Correspondence to Howard Ochman.



The community of microorganisms in an organism or specified environment. The term is often used synonymously with ‘microbiota’ to refer to the taxonomic identity and genomic repertoire of human-associated microbial communities.


A change or perturbation in microbiome composition that differs considerably from that of a control or healthy cohort. The term is frequently used to describe the altered microbiome compositions observed in association with disorders or disease.

Great apes

Members of eight extant species within four genera — Pongo, Gorilla, Pan and Homo — that belong to the family Hominidae. Humans (Homo), gorillas (Gorilla), chimpanzees (Pan) and bonobos (Pan) constitute the African great apes, and orangutans (Pongo) are Asian great apes.


A taxonomic term used to describe unique lineages that are represented by a distinct branch in a phylogenetic tree. In the context of microbiome studies, a phylotype is any sequence that differs by a selected sequence identity threshold, or even a single site, from other sequences.


Characteristic microbial community structures defined by the over-representation of distinct sets of resident bacterial taxa. Originally, the variation in human gut microbiomes appeared to stratify into three enterotypes on the basis of microbial community compositions, although subsequent studies have reported different numbers of gut enterotypes.

Tree topology

The branching order and relationships depicted by a phylogenetic tree.

Vertical inheritance

With regard to microbiomes, the transfer of microorganisms over generations within a host lineage. In human microbiome studies, this describes the transfer of microorganisms from parents and community members to offspring after birth.

Phylogenetic congruency

The matching tree topologies for two different groups of organisms.


Reciprocal changes in organisms of different species that arise owing to their association or interaction, such that each species reciprocally affects the evolution of the other species.


Concurrent diversification of associated or interacting organisms. Cases of co-speciation are usually uncovered by the concordance of the branching orders of the species’ phylogenies. Note that co-evolution may result in co-speciation, but co-speciation can occur in the absence of co-evolution, as would be the case when the co-diversified species are not reciprocally evolving in response to one another.


One species living off the metabolic by-product of another species.

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