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

Research output: Contribution to journalArticlepeer-review

15 Scopus citations

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 mon- keys 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)
Article numbere00271-19
JournalmSphere
Volume4
Issue number4
DOIs
StatePublished - 2019

Bibliographical note

Funding Information:
This publication derives from the HPI-Lab (Laboratory for Infectious Diseases Common to Humans and [non-Human] Primates, Czech Republic), and it was cofinanced by the European Social Fund and state budget of the Czech Republic (project OPVK CZ.1.07/2.3.00/20.0300) and the U.S. National Science Foundation, grant 0935347. This work was partially supported by the Czech-American Scientific cooperation, project number (LH15175), funded by the Ministry of Education, Youth and Sports of The Czech Republic. Uganda Wildlife Authority granted permission for J.M.R. to collect mountain gorilla samples, and Hunter College provided funding. A.G. was supported with funds from the University of Minnesota’s Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT; NIFA project number MN-16-122).

Funding Information:
We thank the government of the Central African Republic and the World Wildlife Fund for granting permission to conduct our research; the Ministre de l'Education Nationale, de l'Alphabetisation, de l'Enseignement Superieur et de la Recherche for providing research permits; and the Primate Habituation Program for providing logistical support in the field. Finally, yet importantly, we thank all of the trackers and assistants in Dzanga Sangha Protected Areas, Central African Republic. This publication derives from the HPI-Lab (Laboratory for Infectious Diseases Common to Humans and [non-Human] Primates, Czech Republic), and it was cofinanced by the European Social Fund and state budget of the Czech Republic (project OPVK CZ.1.07/2.3.00/20.0300) and the U.S. National Science Foundation, grant 0935347. This work was partially supported by the Czech-American Scientific cooperation, project number (LH15175), funded by the Ministry of Education, Youth and Sports of The Czech Republic. Uganda Wildlife Authority granted permission for J.M.R. to collect mountain gorilla samples, and Hunter College provided funding. A.G. was supported with funds from the University of Minnesota's Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT; NIFA project number MN-16-122). A.G. thanks Matt Horowitz, Lyle Kendrick, Thomas Morton, Mike Lopez, Erik Whitestone, and Jerry Ricciotti for useful discussions that inspired ideas to develop the manuscript. A.G. thanks Bolito and Lolo, his most important primates. This work was performed, in part, using computational resources at the Minnesota Supercomputing Institute.

Publisher Copyright:
© 2019 Gomez et al.

Keywords

  • Evolution
  • Microbiome
  • Primate

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