Research Article

Diversity and functional landscapes in the microbiota of animals in the wild

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Science  16 Apr 2021:
Vol. 372, Issue 6539, eabb5352
DOI: 10.1126/science.abb5352

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Mining wild animal microbiomes

We have only just begun to examine the multitude of bacteria associated with other organisms. Levin et al. sampled the feces of 184 wild animals, including fish, birds, and mammals, from four different continents to survey the diversity of gut bacteria (see the Perspective by Lind and Pollard). They discovered more than 1000 previously undescribed bacterial species and identified factors that correlate with the composition, diversity, and functional content of the microbiota. Supporting the association of specific bacteria with animal lifestyle, they identified proteases, some previously undescribed, from the gut of griffon vultures that can break down toxins that may be present in their carrion diet.

Science, this issue p. eabb5352; see also p. 238

Structured Abstract

INTRODUCTION

Animals in the wild are able to subsist on pathogen-infected and poisonous food and show immunity to various diseases. These characteristics may be contributed largely by the animals’ microbiota. However, compared with the human microbiota, which has been extensively studied, the microbiota of animals in the wild has received less focus. In this study, we aimed to construct and functionally annotate a comprehensive database of microbiota sampled from wild animals in their natural habitats. Several considerations guided our sample collection and analysis strategy. First, we focused on sampling of animals from the wild, despite the many challenges that such sampling poses, because captivity was shown to alter the microbiome of several animal species. Second, to obtain a broad representation of wild animals, we sampled in four continents and from a diversity of animals with varied traits and feeding patterns. We hand-curated traits for each species, including dietary adaptations, activity hours, and social structures, allowing us to systematically study the relationships between microbiota composition and host phenotype. Finally, we adapted a metagenomic genome assembly pipeline and annotated the assembled genomes taxonomically and functionally, resulting in a broad collection of genomes that represents the microbial landscape of wildlife.

RATIONALE

It is becoming evident that animal microbiomes are a rich source of biological functions that may have biotechnological impact, including antibiotics, industrial enzymes, and immunomodulators. Moreover, animals in the wild exhibit adaptations such as the safe consumption of rotting, pathogen-infected meat and poisonous plants; production of highly potent toxins; bioluminescence; specific immunity to various diseases and microbial pathogens; regenerative capabilities; and, in some species, extreme longevity. Some of these adaptations, such as toxin production and bioluminescence, are conferred, at least in part, by microbial symbionts living in and on the animal. However, despite these examples, a comprehensive view of the association between an animal’s traits and its microbiota is still lacking. The microbiota of wild animals is also a natural reservoir for pathogens of both animals and humans, the mapping of which could elucidate the timing and routes of their transmission into the human population, as in the case of the current COVID-19 pandemic. Finally, mapping the microbiota of wild animals could also help in conservation efforts.

RESULTS

Our de novo constructed genomes, 75% of which belong to previously undescribed bacterial species, significantly improve the mapping of metagenomic sequencing reads from our animal samples. Notably, the rate at which new genomes are discovered is far from asymptote. We enriched many bacterial phyla with unknown species and found that some bacterial clades have distinctive functional properties relative to other bacteria in the same phylum. We found that the bacterial landscape differs between animal classes and discovered animal class–;specific clusters of coexisting bacteria. We identified multiple pathways and orthologs that are significantly enriched in specific animal traits and showed that the functional landscape is associated with these traits. Some of these functions suggest intriguing new roles and properties of wildlife microbiomes. Moreover, we identified previously undescribed proteases in the microbiota of carrion eaters and show experimentally that they are capable of metabolizing bacterial toxins.

CONCLUSION

Overall, we present a large-scale annotated bacterial genome database of predominantly unknown species that were extracted from the guts of animals in the wild, identified a multitude of microbial patterns that are associated with the traits and taxonomy of these animals, and highlight its potential as a largely untapped resource for the discovery of new industrial enzymes and therapeutics.

A maximum likelihood alignment-based phylogenetic tree of the 1209 genomes assembled in this study.

The inner and outer colored rings denote bacterial phylum and host class, respectively. Clades of previously undescribed genomes are colored dark red.

Abstract

Animals in the wild are able to subsist on pathogen-infected and poisonous food and show immunity to various diseases. These may be due to their microbiota, yet we have a poor understanding of animal microbial diversity and function. We used metagenomics to analyze the gut microbiota of more than 180 species in the wild, covering diverse classes, feeding behaviors, geographies, and traits. Using de novo metagenome assembly, we constructed and functionally annotated a database of more than 5000 genomes, comprising 1209 bacterial species of which 75% are unknown. The microbial composition, diversity, and functional content exhibit associations with animal taxonomy, diet, activity, social structure, and life span. We identify the gut microbiota of wild animals as a largely untapped resource for the discovery of therapeutics and biotechnology applications.

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