Analysis of bacterial genomes from an evolution experiment with horizontal gene transfer shows that recombination can sometimes overwhelm selection

Rohan Maddamsetti,Richard E Lenski,Ivan Matic

doi:10.1371/journal.pgen.1007199

Rohan Maddamsetti, Richard E Lenski + Show 1 more

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https://doi.org/10.1371/journal.pgen.1007199

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Abstract

Few experimental studies have examined the role that sexual recombination plays in bacterial evolution, including the effects of horizontal gene transfer on genome structure. To address this limitation, we analyzed genomes from an experiment in which Escherichia coli K-12 Hfr (high frequency recombination) donors were periodically introduced into 12 evolving populations of E. coli B and allowed to conjugate repeatedly over the course of 1000 generations. Previous analyses of the evolved strains from this experiment showed that recombination did not accelerate adaptation, despite increasing genetic variation relative to asexual controls. However, the resolution in that previous work was limited to only a few genetic markers. We sought to clarify and understand these puzzling results by sequencing complete genomes from each population. The effects of recombination were highly variable: one lineage was mostly derived from the donors, while another acquired almost no donor DNA. In most lineages, some regions showed repeated introgression and others almost none. Regions with high introgression tended to be near the donors’ origin of transfer sites. To determine whether introgressed alleles imposed a genetic load, we extended the experiment for 200 generations without recombination and sequenced whole-population samples. Beneficial alleles in the recipient populations were occasionally driven extinct by maladaptive donor-derived alleles. On balance, our analyses indicate that the plasmid-mediated recombination was sufficiently frequent to drive donor alleles to fixation without providing much, if any, selective advantage.

Highlights

An open question in microbial evolution is why some bacterial taxa seem to have extensive intergenomic recombination [1] while others seem to have little [2]
These mutations arose during the 7000 generations of the long-term evolution experiment (LTEE) that preceded the start of the Souza-Turner-Lenski experiment (STLE), and they persisted for the 1000 generations of the STLE
These K-12 alleles were introduced by intergenomic recombination during the STLE

Summary

Introduction

An open question in microbial evolution is why some bacterial taxa seem to have extensive intergenomic recombination [1] while others seem to have little [2]. Intergenomic recombination can break the linkage between particular beneficial or deleterious mutations and the rest of the genome. Under conditions of high recombination and strong selection, individual genes, rather than entire genomes, can go to fixation. When recombination is infrequent or absent but selection is strong, highly beneficial mutations can drive large genomic regions or even whole genomes to fixation. Recombination in bacteria does not necessarily break up linkage disequilibrium across distant sites on the recipient chromosome; instead, it may preserve a “clonal frame” over most of the chromosome, interrupted by stretches of DNA introduced by horizontal gene transfer [5]

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