Migration and horizontal gene transfer divide microbial genomes into multiple niches.

Rene Niehus,Kevin R. Foster,Alexander G. Fletcher,Sara Mitri

doi:10.1038/ncomms9924

Rene Niehus, Kevin R. Foster + Show 2 more

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https://doi.org/10.1038/ncomms9924

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Abstract

Horizontal gene transfer is central to microbial evolution, because it enables genetic regions to spread horizontally through diverse communities. However, how gene transfer exerts such a strong effect is not understood. Here we develop an eco-evolutionary model and show how genetic transfer, even when rare, can transform the evolution and ecology of microbes. We recapitulate existing models, which suggest that asexual reproduction will overpower horizontal transfer and greatly limit its effects. We then show that allowing immigration completely changes these predictions. With migration, the rates and impacts of horizontal transfer are greatly increased, and transfer is most frequent for loci under positive natural selection. Our analysis explains how ecologically important loci can sweep through competing strains and species. In this way, microbial genomes can evolve to become ecologically diverse where different genomic regions encode for partially overlapping, but distinct, ecologies. Under these conditions ecological species do not exist, because genes, not species, inhabit niches.

Highlights

Horizontal gene transfer is central to microbial evolution, because it enables genetic regions to spread horizontally through diverse communities
When including immigration in our models, we find that the highest rates of horizontal transfer will occur for ecologically important traits that are under positive natural selection
Our models explain how horizontal sweeps of small stretches of DNA can occur in ecologically cohesive communities of microbes

Summary

Introduction

Horizontal gene transfer is central to microbial evolution, because it enables genetic regions to spread horizontally through diverse communities. Our analysis explains how ecologically important loci can sweep through competing strains and species In this way, microbial genomes can evolve to become ecologically diverse where different genomic regions encode for partially overlapping, but distinct, ecologies. Microbes survive and reproduce in an extremely wide range of environments, from hydrothermal vents[1] through marine snow[2] and soil[3], to host associations such as the human microbiome[4] Within and between such environments, microbial genomes differ widely both in terms of allelic diversity and gene content[5,6,7]. At the heart of this genetic diversity is the ability of microbes to gain both homologous and non-homologous DNA via horizontal gene transfer These transfers appear to occur in almost all prokaryotic lineages and have significant impacts on both bacterial and archaeal genomes[8]. The result is a genome where selected regions become partially decoupled from the ecology of the remaining loci such that different parts of the genome map to different niches

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