Dataset Information

Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis.

ABSTRACT: The gut microbiota is recognised as an essential asset for the normal functioning of animal biology. When wild animals are moved into captivity, the modified environmental pressures are expected to rewire the gut microbiota, yet whether this transition follows similar patterns across vertebrates is still unresolved due to the absence of systematic multi-species analyses. We performed a meta-analysis of gut microbiota profiles of 322 captive and 322 wild specimens from 24 vertebrate species. Our analyses yielded no overall pattern of diversity and compositional variation between wild and captive vertebrates, but a heterogeneous landscape of responses, which differed depending on the components of diversity considered. Captive populations showed enrichment patterns of human-associated microorganisms, and the minimal host phylogenetic signal suggests that changes between wild and captive populations are mainly driven by case-specific captivity conditions. Finally, we show that microbiota differences between wild and captive populations can impact evolutionary and ecological inferences that rely on hierarchical clustering-based comparative analyses of gut microbial communities across species.

SUBMITTER: Alberdi A

PROVIDER: S-EPMC8608908 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis.

Alberdi Antton A Martin Bideguren Garazi G Aizpurua Ostaizka O

Scientific reports 20211122 1

The gut microbiota is recognised as an essential asset for the normal functioning of animal biology. When wild animals are moved into captivity, the modified environmental pressures are expected to rewire the gut microbiota, yet whether this transition follows similar patterns across vertebrates is still unresolved due to the absence of systematic multi-species analyses. We performed a meta-analysis of gut microbiota profiles of 322 captive and 322 wild specimens from 24 vertebrate species. Our ...[more]

PMID: 34811423

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Project description:Environmental microbes have harbored the capacity for antibiotic production for millions of years, spanning the evolution of humans and other vertebrates. However, the industrial-scale use of antibiotics in clinical and agricultural practice over the past century has led to a substantial increase in exposure of these agents to human and environmental microbiota. This perturbation is predicted to alter the ecology of microbial communities and to promote the evolution and transfer of antibiotic resistance (AR) genes. We studied wild and captive baboon populations to understand the effects of exposure to humans and human activities (e.g., antibiotic therapy) on the composition of the primate fecal microbiota and the antibiotic-resistant genes that it collectively harbors (the "resistome"). Using a culture-independent metagenomic approach, we identified functional antibiotic resistance genes in the gut microbiota of wild and captive baboon groups and saw marked variation in microbiota architecture and resistomes across habitats and lifeways. Our results support the view that antibiotic resistance is an ancient feature of gut microbial communities and that sharing habitats with humans may have important effects on the structure and function of the primate microbiota. IMPORTANCE Antibiotic exposure results in acute and persistent shifts in the composition and function of microbial communities associated with vertebrate hosts. However, little is known about the state of these communities in the era before the widespread introduction of antibiotics into clinical and agricultural practice. We characterized the fecal microbiota and antibiotic resistomes of wild and captive baboon populations to understand the effect of human exposure and to understand how the primate microbiota may have been altered during the antibiotic era. We used culture-independent and bioinformatics methods to identify functional resistance genes in the guts of wild and captive baboons and show that exposure to humans is associated with changes in microbiota composition and resistome expansion compared to wild baboon groups. Our results suggest that captivity and lifestyle changes associated with human contact can lead to marked changes in the ecology of primate gut communities.

Project description:Captive breeding has been used as an effective approach to protecting endangered animals but its effect on the gut microbiome and the conservation status of these species is largely unknown. The giant panda is a flagship species for the conservation of wildlife. With integrated efforts including captive breeding, this species has been recently upgraded from "endangered" to "vulnerable" (IUCN 2016). Since a large proportion (21.8%) of their global population is still captive, it is critical to understand how captivity changes the gut microbiome of these pandas and how such alterations to the microbiome might affect their future fitness and potential impact on the ecosystem after release into the wild. Here, we use 16S rRNA (ribosomal RNA) marker gene sequencing and shotgun metagenomics sequencing to demonstrate that the fecal microbiomes differ substantially between wild and captive giant pandas. Fecal microbiome diversity was significantly lower in captive pandas, as was the diversity of functional genes. Additionally, captive pandas have reduced functional potential for cellulose degradation but enriched metabolic pathways for starch metabolism, indicating that they may not adapt to a wild diet after being released into the wild since a major component of their diet in the wild will be bamboo. Most significantly, we observed a significantly higher level of amylase activity but a lower level of cellulase activity in captive giant panda feces than those of wild giant pandas, shown by an in vitro experimental assay. Furthermore, antibiotic resistance genes and virulence factors, as well as heavy metal tolerance genes were enriched in the microbiomes of captive pandas, which raises a great concern of spreading these genes to other wild animals and ecosystems when they are released into a wild environment. Our results clearly show that captivity has altered the giant panda microbiome, which could have unintended negative consequences on their adaptability and the ecosystem during the reintroduction of giant pandas into the wild.

Dataset Information

Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis.

Publications

Diversity and compositional changes in the gut microbiota of wild and captive vertebrates: a meta-analysis.

Similar Datasets

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