Robustness of Mammalian Gut Microbiota to Humanization in Captivity.

Brian K. Trevelline,Andrew H. Moeller

doi:10.3389/fevo.2021.785089

Abstract

In mammals, the composition of the gut microbiota is associated with host phylogenetic history, and host-lineage specific microbiota have been shown, in some cases, to contribute to fitness-related traits of their hosts. However, in primates, captivity can disrupt the native microbiota through a process of humanization in which captive hosts acquire gut microbiota constituents found in humans. Despite the potential importance of this process for the health of captive hosts, the degree to which captivity humanizes the gut microbiota of other mammalian taxa has not been explored. Here, we analyzed hundreds of published gut microbiota profiles generated from wild and captive hosts spanning seven mammalian families to investigate the extent of humanization of the gut microbiota in captivity across the mammalian phylogeny. Comparisons of these hosts revealed compositional convergence between captive mammal and human gut microbiota in the majority of mammalian families examined. This convergence was driven by a diversity of microbial lineages, including members of the Archaea, Clostridium, and Bacteroides. However, the gut microbiota of two families—Giraffidae and Bovidae—were remarkably robust to humanization in captivity, showing no evidence of gut microbiota acquisition from humans relative to their wild confamiliars. These results demonstrate that humanization of the gut microbiota is widespread in captive mammals, but that certain mammalian lineages are resistant to colonization by human-associated gut bacteria.

Highlights

The gut microbial communities of wild mammals tend to reflect their hosts’ phylogenetic histories
The gut microbiota of two mammalian families—Giraffidae and Bovidae—were robust to humanization in captivity, showing no evidence of gut microbiota acquisition from humans relative to their wild confamiliars. These results demonstrate that susceptibility of the gut microbiota to humanization appears to be widespread in mammals, but that certain mammalian lineages are resistant to colonization by humanassociated gut bacteria
The combined dataset contained gut microbiota profiles from 657 fecal samples collected from humans and other mammals, including 45,394 Amplicon Sequence Variants (ASVs) represented by 569,790,829 reads

Summary

Introduction

The gut microbial communities of wild mammals tend to reflect their hosts’ phylogenetic histories. There is mounting evidence that certain host-associated microbiota have co-diversified with their hosts (Moeller et al, 2016; Groussin et al, 2017, 2020), indicating the maintenance of specific relationships between gut bacterial and host lineages over evolutionary time These phylogenetic patterns in the gut microbiota suggest the possibility co-evolution and co-adaptation between gut bacteria and mammals, and experimental evidence in rodents has provided some. Germ-free house mice inoculated with non-native gut microbiota from other species of rodent display stunted immune maturation and growth rates relative to germ-free mice inoculated with a native house-mouse microbiota (Chung et al, 2012; Moeller et al, 2019) These studies suggest that disruption of ancient host-microbe associations can result in adverse fitness consequences for the host

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Conclusion