Abstract
Large-scale metagenome assemblies of human microbiomes have produced a vast catalogue of previously unseen microbial genomes; however, comparatively few microbial genomes derive from other vertebrates. Here, we generated 5,596 metagenome-assembled genomes (MAGs) from the gut metagenomes of 180 predominantly wild animal species representing 5 classes, in addition to 14 existing animal gut metagenome data sets. The MAGs comprised 1,522 species-level genome bins (SGBs), most of which were novel at the species, genus, or family level, and the majority were enriched in host versus environment metagenomes. Many traits distinguished SGBs enriched in host or environmental biomes, including the number of antimicrobial resistance genes. We identified 1,986 diverse biosynthetic gene clusters; only 23 clustered with any MIBiG database references. Gene-based assembly revealed tremendous gene diversity, much of it host or environment specific. Our MAG and gene data sets greatly expand the microbial genome repertoire and provide a broad view of microbial adaptations to the vertebrate gut.IMPORTANCE Microbiome studies on a select few mammalian species (e.g., humans, mice, and cattle) have revealed a great deal of novel genomic diversity in the gut microbiome. However, little is known of the microbial diversity in the gut of other vertebrates. We studied the gut microbiomes of a large set of mostly wild animal species consisting of mammals, birds, reptiles, amphibians, and fish. Unfortunately, we found that existing reference databases commonly used for metagenomic analyses failed to capture the microbiome diversity among vertebrates. To increase database representation, we applied advanced metagenome assembly methods to our animal gut data and to many public gut metagenome data sets that had not been used to obtain microbial genomes. Our resulting genome and gene cluster collections comprised a great deal of novel taxonomic and genomic diversity, which we extensively characterized. Our findings substantially expand what is known of microbial genomic diversity in the vertebrate gut.
Highlights
The vertebrate gut microbiome comprises a vast amount of genetic diversity, yet even for the most well-studied species such as humans, the number of microbial species lacking a reference genome was recently estimated to be 40-50%1
Little is known about the distribution of antimicrobial resistance genes in the gut microbiomes of most vertebrate species[27]; we investigated the distribution of AMR genes among MAGs enriched in the environment versus host biomes
While metagenomics is rapidly expanding in popularity[7], most analyses of metagenomic data suffer from a reliance on incomplete reference databases[17], which we show to be acutely problematic for the gut microbiomes of most vertebrates in our dataset
Summary
The vertebrate gut microbiome comprises a vast amount of genetic diversity, yet even for the most well-studied species such as humans, the number of microbial species lacking a reference genome was recently estimated to be 40-50%1. Recent advances in culturomic approaches have generated thousands of novel microbial genomes[4,5,6], but the throughput is currently far outpaced by metagenome assembly approaches[7]. Such large-scale metagenome assembly-based approaches have not been as extensively applied to most non-human vertebrates. The limited number of studies incorporating metagenome assembly hint at the extensive amounts of as-of-yet novel microbial diversity across the >66,000 vertebrate species on our planet
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