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Phenotypic heterogeneity in a bacteriophage population only appears as stress-induced mutagenesis

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Abstract

Stress-induced mutagenesis has been studied in cancer cells, yeast, bacteria, and archaea, but not in viruses. In a recent publication, we present a bacteriophage model showing an apparent stress-induced mutagenesis. We show that the stress does not drive the mutagenesis, but only selects the fittest mutants. The mechanism underlying the observed phenomenon is a phenotypic heterogeneity that resembles persistence of the viral population. The new findings, the background for the ongoing debate on stress-induced mutagenesis, and the phenotypic heterogeneity underlying a novel phage infection strategy are discussed in this short manuscript.

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References

  • Behringer MG, Hall DW (2016) The repeatability of genome-wide mutation rate and spectrum estimates. Curr Genet. doi:10.1007/s00294-016-0573-7

  • Bjedov I, Tenaillon O, Gerard B, Souza V, Denamur E, Radman M, Taddei F, Matic I (2003) Stress-induced mutagenesis in bacteria. Science 300:1404–1409

    Article  CAS  PubMed  Google Scholar 

  • Brauner A, Fridman O, Gefen O, Balaban NQ (2016) Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol 14:320–330

    Article  CAS  PubMed  Google Scholar 

  • Cairns J, Foster PL (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128:695–701

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cairns J, Overbaugh J, Miller S (1988) The origin of mutants. Nature 335:142–145

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1859) On the origin of species by means of natural selection. John Murray, London

    Google Scholar 

  • Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, Hastings PJ (2010) Separate DNA Pol II- and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J Bacteriol 192:4694–4700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galhardo RS, Hastings PJ, Rosenberg SM (2007) Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 42:399–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galhardo RS, Do R, Yamada M, Friedberg EC, Hastings PJ, Nohmi T, Rosenberg SM (2009) DinB upregulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics 182:55–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gefen O, Balaban NQ (2009) The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol Rev 33:704–717

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez C, Hadany L, Ponder RG, Price M, Hastings PJ, Rosenberg SM (2008) Mutability and importance of a hypermutable cell subpopulation that produces stress-induced mutants in Escherichia coli. PLoS Genet 4:e1000208

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamarck JBPA (1809) Philosophie zoologique. Dentu libraire, Paris

    Google Scholar 

  • Lederberg J, Lederberg EM (1952) Replica plating and indirect selection of bacterial mutants. J Bacteriol 63:399–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luria SE, Delbruck M (1943) Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28:491–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maisnier-Patin S, Roth JR (2015) The origin of mutants under selection: how natural selection mimics mutagenesis (adaptive mutation). Cold Spring Harb Perspect Biol 7:a018176

    Article  PubMed  Google Scholar 

  • Newcombe HB (1949) Origin of bacterial variants. Nature 164:150

    Article  CAS  PubMed  Google Scholar 

  • Pettersson ME, Andersson DI, Roth JR, Berg OG (2005) The amplification model for adaptive mutation: simulations and analysis. Genetics 169:1105–1115

    Article  PubMed  PubMed Central  Google Scholar 

  • Pinto D, Mascher T (2016) (Actino)Bacterial “intelligence”: using comparative genomics to unravel the information processing capacities of microbes. Curr Genet. doi:10.1007/s00294-016-0569-3

  • Ponder RG, Fonville NC, Rosenberg SM (2005) A switch from high-fidelity to error-prone DNA double-strand break repair underlies stress-induced mutation. Mol Cell 19:791–804

    Article  CAS  PubMed  Google Scholar 

  • Reams AB, Kofoid E, Kugelberg E, Roth JR (2012) Multiple pathways of duplication formation with and without recombination (RecA) in Salmonella enterica. Genetics 192:397–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roth JR, Andersson DI (2004) Adaptive mutation: how growth under selection stimulates Lac(+) reversion by increasing target copy number. J Bacteriol 186:4855–4860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sano E, Maisnier-Patin S, Aboubechara JP, Quinones-Soto S, Roth JR (2014) Plasmid copy number underlies adaptive mutability in bacteria. Genetics 198:919–933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yosef I, Edgar R, Levy A, Amitai G, Sorek R, Munitz A, Qimron U (2016) Natural selection underlies apparent stress-induced mutagenesis in a bacteriophage infection model. Nat Microbiol. doi:10.1038/nmicrobiol.2016.47

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Acknowledgments

The study was supported by Grants from the European Research Council StG program (336079), the Israel Science Foundation (268/14) and the Israeli Ministry of Health (9988-3).

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Correspondence to Udi Qimron.

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Communicated by M. Kupiec.

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Yosef, I., Edgar, R. & Qimron, U. Phenotypic heterogeneity in a bacteriophage population only appears as stress-induced mutagenesis. Curr Genet 62, 771–773 (2016). https://doi.org/10.1007/s00294-016-0606-2

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  • DOI: https://doi.org/10.1007/s00294-016-0606-2

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