Gene-specific selective sweeps in bacteria and archaea caused by negative frequency-dependent selection.

Nobuto Takeuchi,Otto X Cordero,Kunihiko Kaneko,Eugene V Koonin

doi:10.1186/s12915-015-0131-7

Abstract

BackgroundFixation of beneficial genes in bacteria and archaea (collectively, prokaryotes) is often believed to erase pre-existing genomic diversity through the hitchhiking effect, a phenomenon known as genome-wide selective sweep. Recent studies, however, indicate that beneficial genes spread through a prokaryotic population via recombination without causing genome-wide selective sweeps. These gene-specific selective sweeps seem to be at odds with the existing estimates of recombination rates in prokaryotes, which appear far too low to explain such phenomena.ResultsWe use mathematical modeling to investigate potential solutions to this apparent paradox. Most microbes in nature evolve in heterogeneous, dynamic communities, in which ecological interactions can substantially impact evolution. Here, we focus on the effect of negative frequency-dependent selection (NFDS) such as caused by viral predation (kill-the-winner dynamics). The NFDS maintains multiple genotypes within a population, so that a gene beneficial to every individual would have to spread via recombination, hence a gene-specific selective sweep. However, gene loci affected by NFDS often are located in variable regions of microbial genomes that contain genes involved in the mobility of selfish genetic elements, such as integrases or transposases. Thus, the NFDS-affected loci are likely to experience elevated rates of recombination compared with the other loci. Consequently, these loci might be effectively unlinked from the rest of the genome, so that NFDS would be unable to prevent genome-wide selective sweeps. To address this problem, we analyzed population genetic models of selective sweeps in prokaryotes under NFDS. The results indicate that NFDS can cause gene-specific selective sweeps despite the effect of locally elevated recombination rates, provided NFDS affects more than one locus and the basal rate of recombination is sufficiently low. Although these conditions might seem to contradict the intuition that gene-specific selective sweeps require high recombination rates, they actually decrease the effective rate of recombination at loci affected by NFDS relative to the per-locus basal level, so that NFDS can cause gene-specific selective sweeps.ConclusionBecause many free-living prokaryotes are likely to evolve under NFDS caused by ubiquitous viruses, gene-specific selective sweeps driven by NFDS are expected to be a major, general phenomenon in prokaryotic populations.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0131-7) contains supplementary material, which is available to authorized users.

Highlights

Fixation of beneficial genes in bacteria and archaea is often believed to erase pre-existing genomic diversity through the hitchhiking effect, a phenomenon known as genome-wide selective sweep
Accumulating evidence from ecological and genomic surveys of microbial diversity indicates that archaea and bacteria in nature are organized into genotypic clusters that largely coincide with distinct ecological characteristics [1]
Genome-wide selective sweeps can repeatedly occur in a population adapting to a new environment, each time purging within-population genetic diversity, a phenomenon known as periodic selection [9]

Summary

Introduction

Fixation of beneficial genes in bacteria and archaea (collectively, prokaryotes) is often believed to erase pre-existing genomic diversity through the hitchhiking effect, a phenomenon known as genome-wide selective sweep. Accumulating evidence from ecological and genomic surveys of microbial diversity indicates that archaea and bacteria (collectively, prokaryotes) in nature are organized into genotypic clusters that largely coincide with distinct ecological characteristics [1]. How such patterns of microbial diversity are formed and maintained is an open question in microbial ecology. Takeuchi et al BMC Biology (2015) 13:20 the beneficial gene from the rest of the genome (Figure 1a) This phenomenon is known as genome-wide selective sweep [7] or genetic hitchhiking [8]. Periodic selection makes a population genetically cohesive and distinct from other populations, leading to cluster formation [5]

Methods

Results

Conclusion