A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>

ABSTRACT Bacteria face a trade-off between genetic fidelity, which reduces deleterious mistakes in the genome, and genetic innovation, which allows organisms to adapt. Evidence suggests that many bacteria balance this trade-off by modulating their mutation rates, but few mechanisms have been describ...

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Autores principales:	Nathaniel D. Chu, Sean A. Clarke, Sonia Timberlake, Martin F. Polz, Alan D. Grossman, Eric J. Alm
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e62b4b6e4db14ccfbb1430b04e28a8ca
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spelling	oai:doaj.org-article:e62b4b6e4db14ccfbb1430b04e28a8ca2021-11-15T15:51:06ZA Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>10.1128/mBio.02045-162150-7511https://doaj.org/article/e62b4b6e4db14ccfbb1430b04e28a8ca2017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02045-16https://doaj.org/toc/2150-7511ABSTRACT Bacteria face a trade-off between genetic fidelity, which reduces deleterious mistakes in the genome, and genetic innovation, which allows organisms to adapt. Evidence suggests that many bacteria balance this trade-off by modulating their mutation rates, but few mechanisms have been described for such modulation. Following experimental evolution and whole-genome resequencing of the marine bacterium Vibrio splendidus 12B01, we discovered one such mechanism, which allows this bacterium to switch to an elevated mutation rate. This switch is driven by the excision of a mobile element residing in mutS, which encodes a DNA mismatch repair protein. When integrated within the bacterial genome, the mobile element provides independent promoter and translation start sequences for mutS—different from the bacterium’s original mutS promoter region—which allow the bacterium to make a functional mutS gene product. Excision of this mobile element rejoins the mutS gene with host promoter and translation start sequences but leaves a 2-bp deletion in the mutS sequence, resulting in a frameshift and a hypermutator phenotype. We further identified hundreds of clinical and environmental bacteria across Betaproteobacteria and Gammaproteobacteria that possess putative mobile elements within the same amino acid motif in mutS. In a subset of these bacteria, we detected excision of the element but not a frameshift mutation; the mobile elements leave an intact mutS coding sequence after excision. Our findings reveal a novel mechanism by which one bacterium alters its mutation rate and hint at a possible evolutionary role for mobile elements within mutS in other bacteria. IMPORTANCE DNA mutations are a double-edged sword. Most mutations are harmful; they can scramble precise genetic sequences honed over thousands of generations. However, in rare cases, mutations also produce beneficial new traits that allow populations to adapt to changing environments. Recent evidence suggests that some bacteria balance this trade-off by altering their mutation rates to suit their environment. To date, however, we know of few mechanisms that allow bacteria to change their mutation rates. We describe one such mechanism, driven by the action of a mobile element, in the marine bacterium Vibrio splendidus 12B01. We also found similar mobile genetic sequences in the mutS genes of many different bacteria, including clinical and agricultural pathogens. These mobile elements might play an as yet unknown role in the evolution of these important bacteria.Nathaniel D. ChuSean A. ClarkeSonia TimberlakeMartin F. PolzAlan D. GrossmanEric J. AlmAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Nathaniel D. Chu Sean A. Clarke Sonia Timberlake Martin F. Polz Alan D. Grossman Eric J. Alm A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
description	ABSTRACT Bacteria face a trade-off between genetic fidelity, which reduces deleterious mistakes in the genome, and genetic innovation, which allows organisms to adapt. Evidence suggests that many bacteria balance this trade-off by modulating their mutation rates, but few mechanisms have been described for such modulation. Following experimental evolution and whole-genome resequencing of the marine bacterium Vibrio splendidus 12B01, we discovered one such mechanism, which allows this bacterium to switch to an elevated mutation rate. This switch is driven by the excision of a mobile element residing in mutS, which encodes a DNA mismatch repair protein. When integrated within the bacterial genome, the mobile element provides independent promoter and translation start sequences for mutS—different from the bacterium’s original mutS promoter region—which allow the bacterium to make a functional mutS gene product. Excision of this mobile element rejoins the mutS gene with host promoter and translation start sequences but leaves a 2-bp deletion in the mutS sequence, resulting in a frameshift and a hypermutator phenotype. We further identified hundreds of clinical and environmental bacteria across Betaproteobacteria and Gammaproteobacteria that possess putative mobile elements within the same amino acid motif in mutS. In a subset of these bacteria, we detected excision of the element but not a frameshift mutation; the mobile elements leave an intact mutS coding sequence after excision. Our findings reveal a novel mechanism by which one bacterium alters its mutation rate and hint at a possible evolutionary role for mobile elements within mutS in other bacteria. IMPORTANCE DNA mutations are a double-edged sword. Most mutations are harmful; they can scramble precise genetic sequences honed over thousands of generations. However, in rare cases, mutations also produce beneficial new traits that allow populations to adapt to changing environments. Recent evidence suggests that some bacteria balance this trade-off by altering their mutation rates to suit their environment. To date, however, we know of few mechanisms that allow bacteria to change their mutation rates. We describe one such mechanism, driven by the action of a mobile element, in the marine bacterium Vibrio splendidus 12B01. We also found similar mobile genetic sequences in the mutS genes of many different bacteria, including clinical and agricultural pathogens. These mobile elements might play an as yet unknown role in the evolution of these important bacteria.
format	article
author	Nathaniel D. Chu Sean A. Clarke Sonia Timberlake Martin F. Polz Alan D. Grossman Eric J. Alm
author_facet	Nathaniel D. Chu Sean A. Clarke Sonia Timberlake Martin F. Polz Alan D. Grossman Eric J. Alm
author_sort	Nathaniel D. Chu
title	A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
title_short	A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
title_full	A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
title_fullStr	A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
title_full_unstemmed	A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>
title_sort	mobile element in <italic toggle="yes">muts</italic> drives hypermutation in a marine <italic toggle="yes">vibrio</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/e62b4b6e4db14ccfbb1430b04e28a8ca
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A Mobile Element in <italic toggle="yes">mutS</italic> Drives Hypermutation in a Marine <italic toggle="yes">Vibrio</italic>

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