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.

Highlights

  • Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates

  • While the gut microbiome of populations that rely on westernized subsistence strategies has adapted rapidly to industrialized dietary behaviors and lifestyles [6,7,8], traditional human populations worldwide share numerous compositional and functional traits with nonhuman primates [4, 5, 9]

  • We have shown that when western lowland gorillas transition from dry to wet seasons, their gut microbiome composition corresponds with gut metabolome traits associated with increased energetic turnover [13]

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Summary

Introduction

Compared with urban-industrial populations, small-scale human communities worldwide share a significant number of gut microbiome traits with nonhuman primates. To shed light on the ecological basis of similar and divergent microbiome traits between humans and nonhuman primates, we investigated functional microbiome adaptations to different subsistence strategies in humans and measured the extent to which these adaptations align with those seen in a closely related nonhuman primate across analogous subsistence gradients In this regard, we have previously documented significant compositional microbiome distinctions between the gut microbiomes of sympatric hunter-gatherers and small-scale agriculturalists [7], likely driven by adaptations to process energy-dense, more processed diets by the latter [12]. We discuss our findings in the context of microbiome adaptations to subsistence shifts in humans and nonhuman primates and the factors that shape the human microbiome as we know it today

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