Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 300 (5624): 1404-1409

Copyright © 2003 by the American Association for the Advancement of Science

Stress-Induced Mutagenesis in Bacteria

Ivana Bjedov,1* Olivier Tenaillon,2* Bénédicte Gérard,2* Valeria Souza,3 Erick Denamur,2 Miroslav Radman,1 François Taddei,1 Ivan Matic1{dagger}

Abstract: The evolutionary significance of stress-induced mutagenesis was evaluated by studying mutagenesis in aging colonies (MAC) of Escherichia coli natural isolates. A large fraction of isolates exhibited a strong MAC, and the high MAC variability reflected the diversity of selective pressures in ecological niches. MAC depends on starvation, oxygen, and RpoS and adenosine 3',5'-monophosphate regulons; thus it may be a by-product of genetic strategies for improving survival under stress. MAC could also be selected through beneficial mutations that it generates, as shown by computer modeling and the patterns of stress-inducible and constitutive mutagenesis. We suggest that irrespective of the causes of their emergence, stress-induced mutations participate in adaptive evolution.

1 INSERM U571, Faculté de Médecine Necker-Enfants Malades, Université ParisV, 156 rue Vaugirard, 75730 ParisCedex 15, France.
2 INSERM E0339, Faculté de Médecine Xavier Bichat, Université ParisVII, 16 rue Henri Huchard, 75870 ParisCedex 18, France.
3 Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, México D.F. 04510, México.

Back to Top

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: matic{at}necker.fr


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Chronology in lesion tolerance gives priority to genetic variability.
K. Naiman, G. Philippin, R. P. Fuchs, and V. Pages (2014)
PNAS 111, 5526-5531
   Abstract »    Full Text »    PDF »
Competitive Fitness During Feast and Famine: How SOS DNA Polymerases Influence Physiology and Evolution in Escherichia coli.
C. H. Corzett, M. F. Goodman, and S. E. Finkel (2013)
Genetics 194, 409-420
   Abstract »    Full Text »    PDF »
Effect of the Bacillus atrophaeus subsp. globigii Spo0F H101R Mutation on Strain Fitness.
D. V. Zhelev, M. Hunt, A. Le, C. Dupuis, S. Ren, and H. S. Gibbons (2012)
Appl. Envir. Microbiol. 78, 8601-8610
   Abstract »    Full Text »    PDF »
Competition between Transposable Elements and Mutator Genes in Bacteria.
T. Feher, B. Bogos, O. Mehi, G. Fekete, B. Csorgo, K. Kovacs, G. Posfai, B. Papp, L. D. Hurst, and C. Pal (2012)
Mol. Biol. Evol. 29, 3153-3159
   Abstract »    Full Text »    PDF »
Culture History and Population Heterogeneity as Determinants of Bacterial Adaptation: the Adaptomics of a Single Environmental Transition.
B. Ryall, G. Eydallin, and T. Ferenci (2012)
Microbiol. Mol. Biol. Rev. 76, 597-625
   Abstract »    Full Text »    PDF »
Microbial Scout Hypothesis, Stochastic Exit from Dormancy, and the Nature of Slow Growers.
S. Buerger, A. Spoering, E. Gavrish, C. Leslin, L. Ling, and S. S. Epstein (2012)
Appl. Envir. Microbiol. 78, 3221-3228
   Abstract »    Full Text »    PDF »
Evidence for elevated mutation rates in low-quality genotypes.
N. P. Sharp and A. F. Agrawal (2012)
PNAS 109, 6142-6146
   Abstract »    Full Text »    PDF »
Phenotypic Diversity Caused by Differential RpoS Activity among Environmental Escherichia coli Isolates.
S. M. Chiang, T. Dong, T. A. Edge, and H. E. Schellhorn (2011)
Appl. Envir. Microbiol. 77, 7915-7923
   Abstract »    Full Text »    PDF »
Acceleration of Emergence of Bacterial Antibiotic Resistance in Connected Microenvironments.
Q. Zhang, G. Lambert, D. Liao, H. Kim, K. Robin, C.-k. Tung, N. Pourmand, and R. H. Austin (2011)
Science 333, 1764-1767
   Abstract »    Full Text »    PDF »
Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation in Escherichia coli.
C. Shee, J. L. Gibson, M. C. Darrow, C. Gonzalez, and S. M. Rosenberg (2011)
PNAS 108, 13659-13664
   Abstract »    Full Text »    PDF »
Mutation Rate Inferred From Synonymous Substitutions in a Long-Term Evolution Experiment With Escherichia coli.
S. Wielgoss, J. E. Barrick, O. Tenaillon, S. Cruveiller, B. Chane-Woon-Ming, C. Medigue, R. E. Lenski, D. Schneider, and B. J. Andrews (2011)
g3 1, 183-186
   Abstract »    Full Text »    PDF »
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.
R. L. Frisch, Y. Su, P. C. Thornton, J. L. Gibson, S. M. Rosenberg, and P. J. Hastings (2010)
J. Bacteriol. 192, 4694-4700
   Abstract »    Full Text »    PDF »
Effect of Translesion DNA Polymerases, Endonucleases and RpoS on Mutation Rates in Salmonella typhimurium.
S. Koskiniemi, D. Hughes, and D. I. Andersson (2010)
Genetics 185, 783-795
   Abstract »    Full Text »    PDF »
Noise-Driven Heterogeneity in the Rate of Genetic-Variant Generation as a Basis for Evolvability.
J.-P. Capp (2010)
Genetics 185, 395-404
   Abstract »    Full Text »    PDF »
The Influence of Horizontal Gene Transfer on the Mean Fitness of Unicellular Populations in Static Environments.
Y. Raz and E. Tannenbaum (2010)
Genetics 185, 327-337
   Abstract »    Full Text »    PDF »
Indigenous and Environmental Modulation of Frequencies of Mutation in Lactobacillus plantarum.
R. Machielsen, I. J. van Alen-Boerrigter, L. A. Koole, R. S. Bongers, M. Kleerebezem, and J. E. T. Van Hylckama Vlieg (2010)
Appl. Envir. Microbiol. 76, 1587-1595
   Abstract »    Full Text »    PDF »
Influence of Plasmid pO157 on Escherichia coli O157:H7 Sakai Biofilm Formation.
J. Y. Lim, H. J. La, H. Sheng, L. J. Forney, and C. J. Hovde (2010)
Appl. Envir. Microbiol. 76, 963-966
   Abstract »    Full Text »    PDF »
Letting Escherichia coli Teach Me About Genome Engineering.
J. A. Shapiro (2009)
Genetics 183, 1205-1214
   Abstract »    Full Text »    PDF »
Evolution of Diversity in Spatially Structured Escherichia coli Populations.
J. M. Ponciano, H.-J. La, P. Joyce, and L. J. Forney (2009)
Appl. Envir. Microbiol. 75, 6047-6054
   Abstract »    Full Text »    PDF »
Stress-Induced {beta}-Lactam Antibiotic Resistance Mutation and Sequences of Stationary-Phase Mutations in the Escherichia coli Chromosome.
J. F. Petrosino, R. S. Galhardo, L. D. Morales, and S. M. Rosenberg (2009)
J. Bacteriol. 191, 5881-5889
   Abstract »    Full Text »    PDF »
Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus.
Y. Azuma, A. Hosoyama, M. Matsutani, N. Furuya, H. Horikawa, T. Harada, H. Hirakawa, S. Kuhara, K. Matsushita, N. Fujita, et al. (2009)
Nucleic Acids Res. 37, 5768-5783
   Abstract »    Full Text »    PDF »
Elevated Mutation Frequency in Surviving Populations of Carbon-Starved rpoS-Deficient Pseudomonas putida Is Caused by Reduced Expression of Superoxide Dismutase and Catalase.
K. Tarassova, R. Tegova, A. Tover, R. Teras, M. Tark, S. Saumaa, and M. Kivisaar (2009)
J. Bacteriol. 191, 3604-3614
   Abstract »    Full Text »    PDF »
DinB Upregulation Is the Sole Role of the SOS Response in Stress-Induced Mutagenesis in Escherichia coli.
R. S. Galhardo, R. Do, M. Yamada, E. C. Friedberg, P. J. Hastings, T. Nohmi, and S. M. Rosenberg (2009)
Genetics 182, 55-68
   Abstract »    Full Text »    PDF »
Phage-Associated Mutator Phenotype in Group A Streptococcus.
J. Scott, P. Thompson-Mayberry, S. Lahmamsi, C. J. King, and W. M. McShan (2008)
J. Bacteriol. 190, 6290-6301
   Abstract »    Full Text »    PDF »
Endogenous oxidative stress produces diversity and adaptability in biofilm communities.
B. R. Boles and P. K. Singh (2008)
PNAS 105, 12503-12508
   Abstract »    Full Text »    PDF »
Accumulation of mutants in "aging" bacterial colonies is due to growth under selection, not stress-induced mutagenesis.
M. Wrande, J. R. Roth, and D. Hughes (2008)
PNAS 105, 11863-11868
   Abstract »    Full Text »    PDF »
Hydrogen Peroxide Linked to Lysine Oxidase Activity Facilitates Biofilm Differentiation and Dispersal in Several Gram-Negative Bacteria.
A. Mai-Prochnow, P. Lucas-Elio, S. Egan, T. Thomas, J. S. Webb, A. Sanchez-Amat, and S. Kjelleberg (2008)
J. Bacteriol. 190, 5493-5501
   Abstract »    Full Text »    PDF »
Sexual Selection and Maintenance of Sex: Evidence from Comparisons of Rates of Genomic Accumulation of Mutations and Divergence of Sex-Related Genes in Sexual and Hermaphroditic Species of Caenorhabditis.
C. G. Artieri, W. Haerty, B. P. Gupta, and R. S. Singh (2008)
Mol. Biol. Evol. 25, 972-979
   Abstract »    Full Text »    PDF »
Starvation Induces Genomic Rearrangements and Starvation-Resilient Phenotypes in Yeast.
S. Coyle and E. Kroll (2008)
Mol. Biol. Evol. 25, 310-318
   Abstract »    Full Text »    PDF »
Spontaneous mutation frequency and emergence of ciprofloxacin resistance in Campylobacter jejuni and Campylobacter coli.
M.-L. Hanninen and M. Hannula (2007)
J. Antimicrob. Chemother. 60, 1251-1257
   Abstract »    Full Text »    PDF »
Role of Lon, an ATP-Dependent Protease Homolog, in Resistance of Pseudomonas aeruginosa to Ciprofloxacin.
M. D. Brazas, E. B. M. Breidenstein, J. Overhage, and R. E. W. Hancock (2007)
Antimicrob. Agents Chemother. 51, 4276-4283
   Abstract »    Full Text »    PDF »
Identification of a Novel Streptococcal Gene Cassette Mediating SOS Mutagenesis in Streptococcus uberis.
E. Varhimo, K. Savijoki, J. Jalava, O. P. Kuipers, and P. Varmanen (2007)
J. Bacteriol. 189, 5210-5222
   Abstract »    Full Text »    PDF »
Plasmid incompatibility: more compatible than previously thought?.
N. Velappan, D. Sblattero, L. Chasteen, P. Pavlik, and A. R.M. Bradbury (2007)
Protein Eng. Des. Sel. 20, 309-313
   Abstract »    Full Text »    PDF »
Mutational Bias for Body Size in Rhabditid Nematodes.
D. Ostrow, N. Phillips, A. Avalos, D. Blanton, A. Boggs, T. Keller, L. Levy, J. Rosenbloom, and C. F. Baer (2007)
Genetics 176, 1653-1661
   Abstract »    Full Text »    PDF »
Novel Mutation Assay with High Sensitivity based on Direct Measurement of Genomic DNA Alterations: Comparable Results to the Ames Test.
M. Futakami, M. Salimullah, T. Miura, S. Tokita, and K. Nishigaki (2007)
J. Biochem. 141, 675-686
   Abstract »    Full Text »    PDF »
An editing-defective aminoacyl-tRNA synthetase is mutagenic in aging bacteria via the SOS response.
J. M. Bacher and P. Schimmel (2007)
PNAS 104, 1907-1912
   Abstract »    Full Text »    PDF »
Bone Marrow Failure as a Risk Factor for Clonal Evolution: Prospects for Leukemia Prevention.
G. C. Bagby and G. Meyers (2007)
Hematology 2007, 40-46
   Abstract »    Full Text »    PDF »
Stage-Specific Adaptation of Hypermutable Pseudomonas aeruginosa Isolates during Chronic Pulmonary Infection in Patients with Cystic Fibrosis.
M. Hogardt, C. Hoboth, S. Schmoldt, C. Henke, L. Bader, and J. Heesemann (2007)
The Journal of Infectious Disease 195, 70-80
   Abstract »    Full Text »    PDF »
A paradigm for direct stress-induced mutation in prokaryotes.
J. M. Kang, N. M. Iovine, and M. J. Blaser (2006)
FASEB J 20, 2476-2485
   Abstract »    Full Text »    PDF »
Bacterial metapopulations in nanofabricated landscapes.
J. E. Keymer, P. Galajda, C. Muldoon, S. Park, and R. H. Austin (2006)
PNAS 103, 17290-17295
   Abstract »    Full Text »    PDF »
Cumulative Effects of Spontaneous Mutations for Fitness in Caenorhabditis: Role of Genotype, Environment and Stress.
C. F. Baer, N. Phillips, D. Ostrow, A. Avalos, D. Blanton, A. Boggs, T. Keller, L. Levy, and E. Mezerhane (2006)
Genetics 174, 1387-1395
   Abstract »    Full Text »    PDF »
A Brief History of Systems Biology: "Every object that biology studies is a system of systems." Francois Jacob (1974)..
A. Trewavas (2006)
PLANT CELL 18, 2420-2430
   Full Text »    PDF »
The population dynamics of cancer: a Darwinian perspective.
P. Vineis and M. Berwick (2006)
Int. J. Epidemiol. 35, 1151-1159
   Abstract »    Full Text »    PDF »
Hypermutable bacteria isolated from humans - a critical analysis..
L. M. C. Hall and S. K. Henderson-Begg (2006)
Microbiology 152, 2505-2514
   Abstract »    Full Text »    PDF »
Tuberculosis Chemotherapy: the Influence of Bacillary Stress and Damage Response Pathways on Drug Efficacy.
D. F. Warner and V. Mizrahi (2006)
Clin. Microbiol. Rev. 19, 558-570
   Abstract »    Full Text »    PDF »
Functional Heterogeneity of RpoS in Stress Tolerance of Enterohemorrhagic Escherichia coli Strains.
A. A. Bhagwat, J. Tan, M. Sharma, M. Kothary, S. Low, B. D. Tall, and M. Bhagwat (2006)
Appl. Envir. Microbiol. 72, 4978-4986
   Abstract »    Full Text »    PDF »
Self-engineering capabilities of bacteria.
E. Ben-Jacob and H. Levine (2006)
J R Soc Interface 3, 197-214
   Abstract »    Full Text »    PDF »
The ompA Gene in Chlamydia trachomatis Differs in Phylogeny and Rate of Evolution from Other Regions of the Genome.
B. W. Brunelle and G. F. Sensabaugh (2006)
Infect. Immun. 74, 578-585
   Abstract »    Full Text »    PDF »
Resistance to Antimicrobial Peptides and Stress Response in Mycoplasma pulmonis.
L. F. Fehri, P. Sirand-Pugnet, G. Gourgues, G. Jan, H. Wroblewski, and A. Blanchard (2005)
Antimicrob. Agents Chemother. 49, 4154-4165
   Abstract »    Full Text »    PDF »
Characterization of Colony Morphology Variants Isolated from Pseudomonas aeruginosa Biofilms.
M. J. Kirisits, L. Prost, M. Starkey, and M. R. Parsek (2005)
Appl. Envir. Microbiol. 71, 4809-4821
   Abstract »    Full Text »    PDF »
Up-regulation of competence- but not stress-responsive proteins accompanies an altered metabolic phenotype in Streptococcus mutans biofilms.
C. Rathsam, R. E. Eaton, C. L. Simpson, G. V. Browne, T. Berg, D. W. S. Harty, and N. A. Jacques (2005)
Microbiology 151, 1823-1837
   Abstract »    Full Text »    PDF »
Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation.
A. V Badyaev (2005)
Proc R Soc B 272, 877-886
   Abstract »    Full Text »    PDF »
Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes.
C. F. Baer, F. Shaw, C. Steding, M. Baumgartner, A. Hawkins, A. Houppert, N. Mason, M. Reed, K. Simonelic, W. Woodard, et al. (2005)
PNAS 102, 5785-5790
   Abstract »    Full Text »    PDF »
Bacteriophage and Phenotypic Variation in Pseudomonas aeruginosa Biofilm Development.
J. S. Webb, M. Lau, and S. Kjelleberg (2004)
J. Bacteriol. 186, 8066-8073
   Abstract »    Full Text »    PDF »
High-throughput mutation detection underlying adaptive evolution of Escherichia coli-K12.
C. Honisch, A. Raghunathan, C. R. Cantor, B. O. Palsson, and D. van den Boom (2004)
Genome Res. 14, 2495-2502
   Abstract »    Full Text »    PDF »
An SOS Response Induced by High Pressure in Escherichia coli.
A. Aertsen, R. Van Houdt, K. Vanoirbeek, and C. W. Michiels (2004)
J. Bacteriol. 186, 6133-6141
   Abstract »    Full Text »    PDF »
Adaptive Point Mutation and Adaptive Amplification Pathways in the Escherichia coli Lac System: Stress Responses Producing Genetic Change.
S. M. Rosenberg and P. J. Hastings (2004)
J. Bacteriol. 186, 4838-4843
   Full Text »    PDF »
Involvement of Error-Prone DNA Polymerase IV in Stationary-Phase Mutagenesis in Pseudomonas putida.
R. Tegova, A. Tover, K. Tarassova, M. Tark, and M. Kivisaar (2004)
J. Bacteriol. 186, 2735-2744
   Abstract »    Full Text »    PDF »
Stress-responsive proteins are upregulated in Streptococcus mutans during acid tolerance.
A. C. L. Len, D. W. S. Harty, and N. A. Jacques (2004)
Microbiology 150, 1339-1351
   Abstract »    Full Text »    PDF »
Comment on "High Deleterious Genomic Mutation Rate in Stationary Phase of Escherichia coli".
J. A. G. M. de Visser and D. E. Rozen (2004)
Science 304, 518c
   Full Text »    PDF »
Response to Comment on "High Deleterious Genomic Mutation Rate in Stationary Phase of Escherichia coli".
L. Loewe (2004)
Science 304, 518d
   Full Text »    PDF »
A RecA-LexA-dependent Pathway Mediates Ciprofloxacin-induced Fibronectin Binding in Staphylococcus aureus.
C. Bisognano, W. L. Kelley, T. Estoppey, P. Francois, J. Schrenzel, D. Li, D. P. Lew, D. C. Hooper, A. L. Cheung, and P. Vaudaux (2004)
J. Biol. Chem. 279, 9064-9071
   Abstract »    Full Text »    PDF »
Biased distribution of DNA uptake sequences towards genome maintenance genes.
T. Davidsen, E. A. Rodland, K. Lagesen, E. Seeberg, T. Rognes, and T. Tonjum (2004)
Nucleic Acids Res. 32, 1050-1058
   Abstract »    Full Text »    PDF »
General Stress Response Regulator RpoS in Adaptive Mutation and Amplification in Escherichia coli.
M.-J. Lombardo, I. Aponyi, and S. M. Rosenberg (2004)
Genetics 166, 669-680
   Abstract »    Full Text »    PDF »
Distinct Signatures for Mutator Sensitivity of lacZ Reversions and for the Spectrum of lacI/lacO Forward Mutations on the Chromosome of Nondividing Escherichia coli.
S. M. Bharatan, M. Reddy, and J. Gowrishankar (2004)
Genetics 166, 681-692
   Abstract »    Full Text »    PDF »
The Growth Advantage in Stationary-Phase Phenotype Conferred by rpoS Mutations Is Dependent on the pH and Nutrient Environment.
M. J. Farrell and S. E. Finkel (2003)
J. Bacteriol. 185, 7044-7052
   Abstract »    Full Text »    PDF »
Neutral Mutations and Neutral Substitutions in Bacterial Genomes.
H. Ochman (2003)
Mol. Biol. Evol. 20, 2091-2096
   Abstract »    Full Text »    PDF »
High Deleterious Genomic Mutation Rate in Stationary Phase of Escherichia coli.
L. Loewe, V. Textor, and S. Scherer (2003)
Science 302, 1558-1560
   Abstract »    Full Text »    PDF »
Hypermutation as a Factor Contributing to the Acquisition of Antimicrobial Resistance.
G. M. Eliopoulos and J. Blazquez (2003)
Clinical Infectious Diseases 37, 1201-1209
   Abstract »    Full Text »    PDF »
Nucleoside reverse transcriptase inhibitors and HIV mutagenesis.
N. A. Jewell, R. Chen, R. Raices, and L. M. Mansky (2003)
J. Antimicrob. Chemother. 52, 547-550
   Full Text »    PDF »
MICROBIOLOGY AND EVOLUTION: Modulating Mutation Rates in the Wild.
S. M. Rosenberg and P. J. Hastings (2003)
Science 300, 1382-1383
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882