Traditional human populations and nonhuman primates show parallel gut microbiome adaptations to analogous ecological conditions

Ashok K. Sharma, Klara Petrzelkova, Barbora Pafco, Carolyn A.Jost Robinson, Terence Fuh, Brenda A. Wilson, Rebecca M. Stumpf, Manolito G. Torralba, Ran Blekhman, Bryan White, Karen E. Nelson, Steven R. Leigh, Andres Gomez

Research output: Contribution to journalArticlepeer-review

Abstract

Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates. This overlap is thought to be driven by analogous dietary triggers; however, the ecological and functional bases of this similarity are not fully understood. To start addressing this issue, fecal metagenomes of BaAka hunter-gatherers and traditional Bantu agriculturalists from the Central African Republic were profiled and compared with those of a sympatric western lowland gorilla group (Gorilla gorilla gorilla) across two seasons of variable dietary intake. Results show that gorilla gut microbiomes shared similar functional traits with each human group, depending on seasonal dietary behavior. Specifically, parallel microbiome traits were observed between hunter-gatherers and gorillas when the latter consumed more structural polysaccharides during dry seasons, while small-scale agriculturalist and gorilla microbiomes showed significant functional overlap when gorillas consumed more seasonal ripe fruit during wet seasons. Notably, dominance of microbial transporters, transduction systems, and gut xenobiotic metabolism was observed in association with traditional agriculture and energy-dense diets in gorillas at the expense of a functional microbiome repertoire capable of metabolizing more complex polysaccharides. Differential abundance of bacterial taxa that typically distinguish traditional from industrialized human populations (e.g., Prevotella spp.) was also recapitulated in the human and gorilla groups studied, possibly reflecting the degree of polysaccharide complexity included in each group's dietary niche. These results show conserved functional gut microbiome adaptations to analogous diets in small-scale human populations and nonhuman primates, highlighting the role of plant dietary polysaccharides and diverse environmental exposures in this convergence. IMPORTANCE The results of this study highlight parallel gut microbiome traits in human and nonhuman primates, depending on subsistence strategy. Although these similarities have been reported before, the functional and ecological bases of this convergence are not fully understood. Here, we show that this parallelism is, in part, likely modulated by the complexity of plant carbohydrates consumed and by exposures to diverse xenobiotics of natural and artificial origin. Furthermore, we discuss how divergence from these parallel microbiome traits is typically associated with adverse health outcomes in human populations living under culturally westernized subsistence patterns. This is important information as we trace the specific dietary and environmental triggers associated with the loss and gain of microbial functions as humans adapt to various dietary niches.

Original languageEnglish (US)
Article numbere00815-20
JournalmSystems
Volume5
Issue number6
DOIs
StatePublished - Dec 22 2020

Bibliographical note

Funding Information:
This publication derives from the HPI-Lab (Laboratory for Infectious Diseases Common to Humans and [non-Human] Primates, Czech Republic). Research was cofinanced by the European Social Fund and state budget of the Czech Republic (project OPVK CZ.1.07/2.3.00/20.0300), the U.S. National Science Foundation, grant 0935347, and the Czech-American Scientific cooperation (LH15175) supported by the Ministry of Education, Youth and Sports of The Czech Republic. A.G. and A.K.S. were supported with funds from the University of Minnesota's Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT). Resources from the Minnesota Supercomputing Institute (MSI) at the University of Minnesota were used to conduct all data analyses reported. We would like to express our gratitude to 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. We thank Stephanie Schnorr for her insightful comments to improve the manuscript.

Funding Information:
Research was cofinanced by the European Social Fund and state budget of the Czech Republic (project OPVK CZ.1.07/2.3.00/20.0300), the U.S. National Science Foundation, grant 0935347, and the Czech-American Scientific cooperation (LH15175) supported by the Ministry of Education, Youth and Sports of The Czech Republic. A.G. and A.K.S. were supported with funds from the University of Minnesota’s Agricultural Research, Education, Extension and Technology Transfer Program (AGREETT). Resources from the Minnesota Supercomputing Institute (MSI) at the University of Minnesota were used to conduct all data analyses reported.

Keywords

  • Gorillas
  • Gut microbiome
  • Hunter-gatherers
  • Metagenomics
  • Traditional agriculturalists

PubMed: MeSH publication types

  • Journal Article

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