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

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dc.citation.issue9
dc.citation.volume12
dc.contributor.authorRemigi P
dc.contributor.authorCAPELA D
dc.contributor.authorCLERISSI C
dc.contributor.authorTASSE L
dc.contributor.authorTORCHET R
dc.contributor.authorBOUCHEZ O
dc.contributor.authorBATUT J
dc.contributor.authorCRUVELLIER S
dc.contributor.authorROCHA EPC
dc.contributor.authorMASSON-BOIVIN C
dc.date.available2014-09-01
dc.date.available2014-07-25
dc.date.issued2014-09
dc.description.abstractHorizontal gene transfer (HGT) is an important mode of adaptation and diversification of prokaryotes and eukaryotes and a major event underlying the emergence of bacterial pathogens and mutualists. Yet it remains unclear how complex phenotypic traits such as the ability to fix nitrogen with legumes have successfully spread over large phylogenetic distances. Here we show, using experimental evolution coupled with whole genome sequencing, that co-transfer of imuABC error-prone DNA polymerase genes with key symbiotic genes accelerates the evolution of a soil bacterium into a legume symbiont. Following introduction of the symbiotic plasmid of Cupriavidus taiwanensis, the Mimosa symbiont, into pathogenic Ralstonia solanacearum we challenged transconjugants to become Mimosa symbionts through serial plant-bacteria co-cultures. We demonstrate that a mutagenesis imuABC cassette encoded on the C. taiwanensis symbiotic plasmid triggered a transient hypermutability stage in R. solanacearum transconjugants that occurred before the cells entered the plant. The generated burst in genetic diversity accelerated symbiotic adaptation of the recipient genome under plant selection pressure, presumably by improving the exploration of the fitness landscape. Finally, we show that plasmid imuABC cassettes are over-represented in rhizobial lineages harboring symbiotic plasmids. Our findings shed light on a mechanism that may have facilitated the dissemination of symbiotic competency among α- and β-proteobacteria in natura and provide evidence for the positive role of environment-induced mutagenesis in the acquisition of a complex lifestyle trait. We speculate that co-transfer of complex phenotypic traits with mutagenesis determinants might frequently enhance the ecological success of HGT.
dc.description.publication-statusPublished
dc.format.extent? - ? (12)
dc.identifierhttp://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000342905400004&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=c5bb3b2499afac691c2e3c1a83ef6fef
dc.identifierARTN e1001942
dc.identifier.citationPLOS BIOLOGY, 2014, 12 (9), pp. ? - ? (12)
dc.identifier.doi10.1371/journal.pbio.1001942
dc.identifier.elements-id239435
dc.identifier.harvestedMassey_Dark
dc.identifier.issn1545-7885
dc.languageEnglish
dc.publisherPublic Library of Science
dc.relation.isPartOfPLOS BIOLOGY
dc.rights2014 Remigi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
dc.subjectScience & Technology
dc.subjectLife Sciences & Biomedicine
dc.subjectBiochemistry & Molecular Biology
dc.subjectBiology
dc.subjectLife Sciences & Biomedicine - Other Topics
dc.subjectSTRESS-INDUCED MUTAGENESIS
dc.subjectMYCOBACTERIUM-TUBERCULOSIS
dc.subjectSINORHIZOBIUM-MELILOTI
dc.subjectRHIZOBIUM-RHIZOGENES
dc.subjectFLUCTUATION ANALYSIS
dc.subjectSHIGELLA-FLEXNERI
dc.subjectESCHERICHIA-COLI
dc.subjectBACTERIA
dc.subjectSYMBIOSIS
dc.subjectGENOME
dc.subject.anzsrc06 Biological Sciences
dc.subject.anzsrc07 Agricultural and Veterinary Sciences
dc.subject.anzsrc11 Medical and Health Sciences
dc.titleTransient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer
dc.typeJournal article
pubs.notesNot known
pubs.organisational-group/Massey University
pubs.organisational-group/Massey University/College of Sciences
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