TitleA Mobile Element in mutS Drives Hypermutation in a Marine Vibrio.
Publication TypeJournal Article
AuthorsChu ND, Clarke SA, Timberlake S, Polz MF, Grossman AD, Alm EJ
Date2017 Feb 07
KeywordsAquatic Organisms, Interspersed Repetitive Sequences, Mutagenesis, Insertional, Mutation Rate, MutS DNA Mismatch-Binding Protein, Recombination, Genetic, Vibrio

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.

Alternate JournalMBio
PubMed ID28174306
PubMed Central IDPMC5296598
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    <p><strong>Professor Martin Polz</strong><br>Ralph M. Parsons Laboratory for Environmental Science and Engineering<br>Massachusetts Institute of Technology<br>15 Vassar Street, Bldg 48-417<br>Cambridge, MA 02139</p>
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    Microbial Ecology and Evolution
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    Environmental microbiology is at an important crossroads. Over the last twenty years we have learned that microbes are the most ubiquitous organisms on Earth, yet the dynamics that govern their interactions and evolution remain poorly understood. What is the role of individual populations within the community? What is the range of genomic similarity that defines a population as a functional unit? What mechanisms govern diversification of microbial populations in the environment?

    We address these questions using a combination of quantitative molecular approaches, genomics, physiology, and modeling. Our primary model system is the coastal ocean where we study patterns of diversity among co-occurring bacterioplankton from the level of the entire community to the individual genome. For the latter, we focus on bacteria of the genus Vibrio, which are longstanding models of heterotrophic, marine bacteria and also contain many pathogenic variants (e.g., V. choleraeV. vulnificus). As part of the Woods Hole Center for Oceans and Human Health (COHH), we are also exploring environmental and evolutionary mechanisms that trigger the emergence of pathogenic variants within the vibrios.  We are also part of the Earth Systems Initiative and the Microbial Systems Group at MIT.

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