Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints

Andres Gomez, Ashok Kumar Sharma, Elizabeth K. Mallott, Klara J. Petrzelkova, Carolyn A. Jost Robinson, Carl J. Yeoman, Franck Carbonero, Barbora Pafco, Jessica M. Rothman, Alexander Ulanov, Klara Vlckova, Katherine R. Amato, Stephanie L. Schnorr, Nathaniel J. Dominy, David Modry, Angelique Todd, Manolito Torralba, Karen E. Nelson, Michael B. Burns, Ran BlekhmanMelissa Remis, Rebecca M. Stumpf, Brenda A. Wilson, H. Rex Gaskins, Paul A. Garber, Bryan A. White, Steven R. Leigh, Katherine Mcmahon

Research output: Contribution to journalArticle

Abstract

The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets.
Original languageEnglish (US)
Number of pages14
JournalmSphere
Volume4
Issue number4
DOIs
StatePublished - Jul 31 2019

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Microbiota
Primates
Haplorhini
Cercopithecidae
Population
Diet
Hominidae
Gastrointestinal Microbiome
Life Style
History

Cite this

Gomez, A., Sharma, A. K., Mallott, E. K., Petrzelkova, K. J., Jost Robinson, C. A., Yeoman, C. J., ... Mcmahon, K. (2019). Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints. mSphere, 4(4). https://doi.org/10.1128/mSphere.00271-19

Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints. / Gomez, Andres; Sharma, Ashok Kumar; Mallott, Elizabeth K.; Petrzelkova, Klara J.; Jost Robinson, Carolyn A.; Yeoman, Carl J.; Carbonero, Franck; Pafco, Barbora; Rothman, Jessica M.; Ulanov, Alexander; Vlckova, Klara; Amato, Katherine R.; Schnorr, Stephanie L.; Dominy, Nathaniel J.; Modry, David; Todd, Angelique; Torralba, Manolito; Nelson, Karen E.; Burns, Michael B.; Blekhman, Ran; Remis, Melissa; Stumpf, Rebecca M.; Wilson, Brenda A.; Gaskins, H. Rex; Garber, Paul A.; White, Bryan A.; Leigh, Steven R.; Mcmahon, Katherine.

In: mSphere, Vol. 4, No. 4, 31.07.2019.

Research output: Contribution to journalArticle

Gomez, A, Sharma, AK, Mallott, EK, Petrzelkova, KJ, Jost Robinson, CA, Yeoman, CJ, Carbonero, F, Pafco, B, Rothman, JM, Ulanov, A, Vlckova, K, Amato, KR, Schnorr, SL, Dominy, NJ, Modry, D, Todd, A, Torralba, M, Nelson, KE, Burns, MB, Blekhman, R, Remis, M, Stumpf, RM, Wilson, BA, Gaskins, HR, Garber, PA, White, BA, Leigh, SR & Mcmahon, K 2019, 'Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints', mSphere, vol. 4, no. 4. https://doi.org/10.1128/mSphere.00271-19
Gomez A, Sharma AK, Mallott EK, Petrzelkova KJ, Jost Robinson CA, Yeoman CJ et al. Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints. mSphere. 2019 Jul 31;4(4). https://doi.org/10.1128/mSphere.00271-19
Gomez, Andres ; Sharma, Ashok Kumar ; Mallott, Elizabeth K. ; Petrzelkova, Klara J. ; Jost Robinson, Carolyn A. ; Yeoman, Carl J. ; Carbonero, Franck ; Pafco, Barbora ; Rothman, Jessica M. ; Ulanov, Alexander ; Vlckova, Klara ; Amato, Katherine R. ; Schnorr, Stephanie L. ; Dominy, Nathaniel J. ; Modry, David ; Todd, Angelique ; Torralba, Manolito ; Nelson, Karen E. ; Burns, Michael B. ; Blekhman, Ran ; Remis, Melissa ; Stumpf, Rebecca M. ; Wilson, Brenda A. ; Gaskins, H. Rex ; Garber, Paul A. ; White, Bryan A. ; Leigh, Steven R. ; Mcmahon, Katherine. / Plasticity in the Human Gut Microbiome Defies Evolutionary Constraints. In: mSphere. 2019 ; Vol. 4, No. 4.
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abstract = "The gut microbiome of primates, including humans, is reported to closely follow host evolutionary history, with gut microbiome composition being specific to the genetic background of its primate host. However, the comparative models used to date have mainly included a limited set of closely related primates. To further understand the forces that shape the primate gut microbiome, with reference to human populations, we expanded the comparative analysis of variation among gut microbiome compositions and their primate hosts, including 9 different primate species and 4 human groups characterized by a diverse set of subsistence patterns (n = 448 samples). The results show that the taxonomic composition of the human gut microbiome, at the genus level, exhibits increased compositional plasticity. Specifically, we show unexpected similarities between African Old World monkeys that rely on eclectic foraging and human populations engaging in nonindustrial subsistence patterns; these similarities transcend host phylogenetic constraints. Thus, instead of following evolutionary trends that would make their microbiomes more similar to that of conspecifics or more phylogenetically similar apes, gut microbiome composition in humans from nonindustrial populations resembles that of generalist cercopithecine monkeys. We also document that wild cercopithecine monkeys with eclectic diets and humans following nonindustrial subsistence patterns harbor high gut microbiome diversity that is not only higher than that seen in humans engaging in industrialized lifestyles but also higher compared to wild primates that typically consume fiber-rich diets.",
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AU - Jost Robinson, Carolyn A.

AU - Yeoman, Carl J.

AU - Carbonero, Franck

AU - Pafco, Barbora

AU - Rothman, Jessica M.

AU - Ulanov, Alexander

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AU - Todd, Angelique

AU - Torralba, Manolito

AU - Nelson, Karen E.

AU - Burns, Michael B.

AU - Blekhman, Ran

AU - Remis, Melissa

AU - Stumpf, Rebecca M.

AU - Wilson, Brenda A.

AU - Gaskins, H. Rex

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AU - White, Bryan A.

AU - Leigh, Steven R.

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