Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer.

Philippe Remigi,Rachel Torchet,Eduardo P C Rocha,Camille Clerissi,Stéphane Cruveiller,Jacques Batut,Olivier Bouchez,Catherine Masson-Boivin,Léna Tasse,Delphine Capela

doi:10.1371/journal.pbio.1001942

Abstract

Author SummaryHorizontal gene transfer has an extraordinary impact on microbe evolution and diversification, by allowing exploration of new niches such as higher organisms. This is the case for rhizobia, a group of phylogenetically diverse bacteria that form a nitrogen-fixing symbiotic relationship with most leguminous plants. While these arose through horizontal transfer of symbiotic plasmids, this in itself is usually unproductive, and full expression of the acquired traits needs subsequent remodeling of the genome to ensure the ecological success of the transfer. Here we uncover a mechanism that accelerates the evolution of a soil bacterium into a legume symbiont. We show that key symbiotic genes are co-transferred with genes encoding stress-responsive error-prone DNA polymerases that transiently elevate the mutation rate in the recipient genome. This burst in genetic diversity accelerates the symbiotic evolution process under selection pressure from the host plant. A more widespread involvement of plasmid mutagenesis cassettes in rhizobium evolution is supported by their overrepresentation in rhizobia-containing lineages. Our findings provide evidence for the role of environment-induced mutagenesis in the acquisition of a complex lifestyle trait and predict that co-transfer of complex phenotypic traits with mutagenesis determinants might help successful horizontal gene transfer.

Highlights

Horizontal gene transfer (HGT) drives bacterial ecological diversification by providing genomes with new genes and functions [1,2,3,4]
Fluctuation tests [27], which allow measuring the mutation rate of growing bacteria, confirmed that neither the chimeric ancestor GMI1000pRalta nor the three first nodulating clones CBM212, CBM349, and CBM356 (Figure 1A) were constitutive hypermutators (Figure S1). These results suggest that transient hypermutagenesis generated genetic diversity during the evolution experiment
In each cycle plants in tubes were inoculated with bacteria, which diffused in the carbon-free and nitrogen-free plant culture Jensen medium before entering the root and multiplying within the newly induced nodules (Figure 1E)

Summary

Introduction

Horizontal gene transfer (HGT) drives bacterial ecological diversification by providing genomes with new genes and functions [1,2,3,4]. The high virulence of Shigella flexneri and Vibrio cholerae results directly from the acquisition of virulence factors in mobile genetic elements [7,8]. Mobile elements confer traits that are involved in the establishment of mutualistic associations [9]. Many mobile genetic elements have narrow-host ranges and this favors horizontal transfer between closely related bacteria [10]. Transfer is more likely to be successful when it concerns simple traits and takes place between closely related bacteria because this increases the probability of gene expression and integration in the host genetic background [11,12]. Genetic transfer of complex traits between very distantly related taxa has an important role in bacterial evolution [13]. Acquisition of type 3 secretion systems by plant-associated pathogenic bacteria was followed by the replacement of the Author Summary

Methods

Results

Conclusion