Stationary phase mutagenesis: Mechanisms that accelerate adaptation of microbial populations under environmental stress

Environmental Microbiology

Volumn 5, Issue 10, 2003, Pages 814-827

  Kivisaar, Maia ^a  

^a UNIVERSITY OF TARTU   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA DIRECTED DNA POLYMERASE;

ADAPTATION; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIUM; DNA REPAIR; ENVIRONMENT; EVOLUTION; GENETICS; METABOLISM; MUTAGENESIS; SHORT SURVEY;

ADAPTATION, BIOLOGICAL; BACTERIA; BACTERIAL PHYSIOLOGY; BACTERIAL PROTEINS; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; ENVIRONMENT; EVOLUTION; MUTAGENESIS;

BACTERIA (MICROORGANISMS);

EID: 0141453385     PISSN: 14622912     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-2920.2003.00488.x     Document Type: Short Survey

References (162)

1. Aldén, L., Demoling, F., and Bååth, E. (2001) Rapid method of determining factors limiting bacterial growth in soil. Appl Environ Microbiol 67: 1830-1838.
2. Andersson, D.I., Slechta, E.S., and Roth, J.R. (1998) Evidence that gene amplification underlies adaptive mutability of the bacterial lac operon. Science 282: 1133-1135.
3. Au, K.G., Welsh, K., and Modrich, P. (1992) Initiation of methyl-directed mismatch repair. J Biol Chem 267: 12142-12148.
4. Bååth, E. (1998) Growth rates of bacterial communities in soils at varying pH: a comparison of the thymidine and leucine incorporation techniques. Microb Ecol 36: 316-327.
5. Bayliss, C.D., Field, D., and Moxon, R.E. (2001) The simple sequence contingency loci of Haemophilus influenzae and Neisseria meningitides. J Clin Invest 107: 657-662.
6. Bhamre, S., Gadea, B.B., Koyama, C.A., White, S.J., and Fowler, R.G. (2001) An aerobic recA-, umuC,- dependent pathway of spontaneous base-pair substitution mutagenesis in Escherichia coli. Mutat Res 473: 229-147.
7. Biel, S.W., and Hartl, D.L. (1983) Evolution of transposons: natural selection for Tn5. Escherichia coli K12. Genetics 103: 581-592.
8. Brenner, S., and Milstein, C. (1966) Origin of antibody variation. Nature 211: 242-243.
9. Bridges, B.A. (1997) Hypermutation under stress. Nature 387: 557-558.
10. Bridges, B.A., Sekiguchi, M., and Tajiri, T. (1996) Effect of mutY and mutM/fpg-1 mutations on starvation-associated mutation in Escherichia coli: implications for the role of 7,8-dihydro-8-oxoguanine. Mol Gen Genet 251: 352-357.
11. Brown, E.W., LeClerc, J.E., Li, B., Payne, W.L., and Cebula, T.A. (2001) Phylogenetic evidence for horizontal transfer of mutS alleles among naturally occurring Escherichia coli strains. J Bacteriol 183: 1631-1644.
12. Bull, H.J., Lombardo, M.-J., and Rosenberg, S.M. (2001) Stationary-phase mutation in the bacterial chromosome: recombination protein and DNA polymerase IV dependence. Proc Natl Acad Sci USA 98: 8334-8341.
13. Cairns, J. (1998) Mutation and cancer: the antecedents to our studies of adaptive mutation. Genetics 148: 1433-1440.
14. Cairns, J., and Foster, P.L. (1991) Adaptive reversion of a frameshift mutation in Escherichia coli. Genetics 128: 695-701.
15. Chao, L., and McBroom, S.M. (1985) Evolution of transposable elements: an IS 10 insertion increases fitness in Escherichia coli. Mol Biol Evol 2: 359-369.
16. Chao, L., Vargas, C., Spear, B.B., and Cox, E.C. (1983) Transposable elements as mutator genes in evolution. Nature 303: 633-635.
17. Claverys, J.-P., Prudhomme, M., Mortier-Barriére and Martin, B. (2000) Adaptation to the environment: Streptococcus pneumoniae, a paradigm for recombination-mediated genetic plasticity? Mol Microbiol 35: 251-259.
18. De Bolle, X., Bayliss, C.D., Field, D., van de Ven, T., Saunders, N.J., Hood, D.W., and Moxon, E.R. (2000) The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol Microbiol 35: 211-222.
19. Denamur, E., Lecointre, G., Darlu, P., Tenaillon, O., Acquaviva, C., Sayada, C., et al. (2000) Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell 103: 711-721.
20. Déziel, E., Comeau, Y., and Villemur, R. (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204.
21. Di Noia, J., and Neuberger, M.S. (2002) Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature 419: 43-48.
22. Diaz, M., Verkoczy, L.K., Flajnik, M.F., and Klinman, N.R. (2001) Decreased frequency of somatic hypermutation and impaired affinity maturation but intact germinal center formation in mice expressing antisense RNA to DNA polymerase ζ. J Immunol 167: 327-335.
23. Doolittle, W.F., and Sapienza, C. (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601-603.
24. Drake, J.W. (1991) Spontaneous mutation. Annu Rev Genet 25: 125-146.
25. Drenkard, E., and Ausubel, F.M. (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743.
26. Eichenbaum, Z., and Livneh, Z. (1998) UV light induces IS 10 transposition in Escherichia coli. Genetics 149: 1173-1181.
27. Faili, A., Aoufouchi, S., Flatter, E., Guéranger, Q., Reynaud, C.-A., and Weill, J.-C. (2002) Induction of somatic hypermutation in immunoglobulin genes is dependent on DNA polymerase iota. Nature 419: 944-947.
28. Feng, G., Tsui, H.-C.T., and Winkler, M.E. (1996) Depletion of the cellular amounts of the MutS and MutH methyl-directed mismatch repair proteins in stationary-phase Escherichia coli K-12 cells. J Bacteriol 178: 2388-2396.
29. Finkel, S.E., Zinser, E.R., and Kolter, R. (2000) Long-term survival and evolution in the stationary phase. In Bacterial Stress Responses. Storz, G., and Hengge-Aronis, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 231-138.
30. Foster, P.L. (1997) Nonadaptive mutations occur on the F′ episome during adaptive mutation conditions in Escherichia coli. J Bacteriol 179: 1550-1554.
31. Foster, P.L. (1999a) Mechanisms of stationary phase mutation: a decade of adaptive mutation. Annu Rev Genet 33: 57-88.
32. Foster, P.L. (1999b) Are adaptive mutations due to a decline in mismatch repair? The evidence is lacking. Mutat Res 436: 179-184.
33. Foster, P.L. (2000) Adaptive mutation: implications for evolution. Bioessays 22: 1067-1074.
34. Foster, P.L., and Trimarchi, J.M. (1994) Adaptive reversion of a frameshift mutation in Escherichia coli by simple base deletions in homopolymeric runs. Science 265: 407-409.
35. Foster, P.L., and Trimarchi, J.M. (1995) Adaptive reversion of an episomal frameshift mutation in Escherichia coli requires conjugal functions but not actual conjugation. Proc Natl Acad Sci USA 92: 5487-5490.
36. Foster, P.L., Trimarchi, J.M., and Maurer, R.A. (1996) Two enzymes, both of which process recombination intermediates, have opposite effects on adaptive mutation in Escherichia coli. Genetics 142: 25-37.
37. Frank, E.G., Tissier, A., McDonald, J.P., Rapić-Otrin, V., Zeng, X., Gearhart, P.J., and Woodgate, R. (2001) Altered nucleotide misinsertion fidelity associated with poli-dependent replication at the end of a DNA template. EMBO J 20: 2914-2922.
38. Friedberg, E.C., Walker, G.C., and Siede, W. (1995) DNA Repair and Mutagenesis. Washington, DC: American Society for Microbiology Press.
39. Friedberg, E.C., Wagner, R., and Radman, M. (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations. Science 296: 1627-1630.
40. Funchain, P., Yeung, A., Stewart, J.L., Lin, R., Slupska, M.M., and Miller, J.H. (2000) The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154: 959-970.
41. Galas, D.J., and Chandler, M. (1989) Bacterial insertion sequences. In Mobile DNA. Berg, D.E., and Howe, M.H. (eds). Washington, DC: American Society for Microbiology Press, pp. 109-162.
42. Gearhart, P.J. (2002) The roots of antibody diversity. Nature 419: 29-31.
43. Gearhart, P.J., and Bogenhagen, D.F. (1983) Clusters of point mutations are found exclusively around rearranged antibody variable genes. Proc Natl Acad Sci USA 80: 3439-3943.
44. Gearhart, P.J., and Wood, R.D. (2001) Emerging links between hypermutation of antibody genes and DNA polymerases. Nature Rev Immunol 1: 187-192.
45. Giraud, A., Matic, I., Tenaillon, O., Clara, A., Radman, M., Fons, M., and Taddei, F. (2001) Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291: 2606-2608.
46. Godoy, V.G., Gizatullin, F.S., and Fox, M.S. (2000) Some features of the mutability of bacteria during nonlethal selection. Genetics 154: 49-59.
47. + mutants of Escherichia coli MCS2. J Bacteriol 179: 4620-4622.
48. Goodman, M.F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 71: 17-50.
49. Grilley, M., Welsh, K.M., Su, S.S., and Modrich, P. (1989) Isolation and characterization of Escherichia coli mutL gene product. J Biol Chem 264: 1000-1004.
50. Gsell, T.C., Holben, W.E., and Ventullo, R.M. (1997) Characterization of the sediment bacterial community in groundwater discharge zones of an alkaline fen: a seasonal study. Appl Environ Microbiol 63: 3111-3118.
51. Hall, B.G. (1988) Adaptive evolution that requires multiple spontaneous mutations. I. Mutations ir volving an insertion sequence. Genetics 120: 887-897.
52. Hall, B.G. (1990) Spontaneous point mutations that occur more often when they are advantageous than when they are neutral. Genetics 126: 5-16.
53. Hall, B.G. (1995) Adaptive mutations in Escherichia coli as a model for the multiple mutational origins of tumors. Proc Natl Acad Sci USA 92: 5669-5673.
54. Hall, B.G. (1998) Adaptive mutagenesis: a process that generates almost exclusively beneficial mutations. Genetica 102/103: 109-125.
55. Harfe, B.D., and Jinks-Robertson, S. (2000) DNA mismatch repair and genetic instability. Annu Rev Genet 34: 359-399.
56. Harris, R.S., Ross, K.J., and Rosenberg, S.M. (1996) Opposing roles of Holliday junction processing systems of Escherichia coli in recombination-dependent adaptive mutation. Genetics 142: 681-691.
57. Harris, R.S., Feng, G., Ross, K.J., Sidhu, R., Thulin, C., Longerich, S., et al. (1997) Mismatch repair protein MutL becomes limiting during stationary-phase mutation. Genes Dev 11: 2426-2437.
58. Harris, R.S., Feng, G., Ross, K.J., Sidhu, R., Thulin, C., Longerich, S., et al. (1999a) Mismatch repair is diminished during stationary-phase mutation. Mutat Res 437: 51-60.
59. Harris, R.S., Kong, Q., and Maizels, N. (1999b) Somatic hypermutation and the three R's: repair, replication and recombination. Mutat Res 436: 157-178.
60. Harris, R.S., Sale, J.E., Petersen-Mahrt, S.K., and Neuberger, M.S. (2002) AID is essential for immunoglobulin V gene conversion in a cultured B cell line. Curr Biol 12: 435-438.
61. Hastings, P.J., and Rosenberg, S.M. (2002) In pursuit of a molecular mechanism for adaptive gene amplification. DNA Repair 1: 111-123.
62. Heijnen, C.E., Page, S., and van Elsas, J.D. (1995) Metabolic activity of Flavobacterium strain P25 during starvation and after introduction into bulk soil and the rhizosphere of wheat. FEMS Microbiol Ecol 18: 129-138.
63. Henderson, I.R., Owen, P., and Nataro, J.P. (1999) Molecular switches - the ON and OFF of bacterial phase variation. Mol Microbiol 33: 919-932.
64. Hendrickson, H., Slechta, E.S., Bergthorsson, U., Andersson, D.I., and Roth, J.R. (2002) Amplification-mutagenesis: evidence that 'directed' adaptive mutation and general hypermutability result from growth with a selected gene amplification. Proc Natl Acad Sci USA 99: 2164-2169.
65. Hughes, D., and Andersson, D.I. (1997) Carbon starvation of Salmonella typhimurium does not ca use general increase of mutation rates. J Bacteriol 179: 6688-6691.
66. Humbert, O., Prudhomme, M., Hakenbeck, R., Dowson, C.G., and Claverys, J.-P. (1995) Homologous recombination and mismatch repair during transformation in Streptococcus pneumoniae: saturation of the Hex mismatch repair system. Proc Natl Acad Sci USA 92: 9052-9056.
67. s in starvation-induced transposition of Pseudomonas putida transposon Tn4652. J Bacteriol 183: 5445-5448.
68. Jiang, N., Bao, Z., Zhang, X., Hirochika, H., Eddy, S.R., McCouch, S.R., and Wessler, S.R. (2003) An active DNA transposon in rice. Nature 421: 163-166.
69. Kasak, L., Hõrak, R., and Kivisaar, M. (1997) Promoter-creating mutations in Pseudomonas putida: a model system for the study of mutation in starving bacteria. Proc Natl Acad Sci USA 94: 3134-3139.
70. Kidwell, M.G., and Lisch, D.R. (2002) Transposable elements as sources of genomic variation. In Mobile DNA II. Craig, N.L., Craigie, R., Gellert, M., and Lambowitz, A.M. (eds). Washington, DC: American Society for Microbiology Press, pp. 59-90.
71. Kim, S.-R., Maenhaut-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., et al. (1997) Multiple pathways for SOS-induced mutagenesis in Eschericha coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci USA 94: 13792-13797.
72. Kim, W.S., Park, J.H., Ren, J., Su, P., and Dunn, N.W. (2001) Survival response and rearrangement of plasmid DNA of Lactococcus lactis during long-term starvation. Appl Environ Microbiol 67: 4594-4602.
73. s-dependent gene expression in Pseudomonas fluorescens, soil. Appl Environ Microbiol 67: 3363-3370.
74. 128 pro lac). J Bacteriol 185: 660-663.
75. Kokjohn, T.A., and Miller, R.V. (1994) IncN plasmids mediate UV resistance and error-prone repair in Pseudomonas aeruginosa PAO. Microbiology 140: 43-48.
76. Kramer, J.G., and Singleton, F.L. (1992) Variations in rRNA content of marine Vibrio spp. during starvation-survival and recovery. Appl Environ Microbiol 58: 201-207.
77. Lamrani, S., Ranquet, C., Gama, M.-J., Nakai, H., Shapiro, J.A., Toussaint, A., and Maenhaut-Michel, G. (1999) Starvation-induced Mucts62-mediated coding sequence fusion: a role for CIpXP, Lon, RpoS and Crp. Mol Microbiol 32: 327-343.
78. LeClerc, J.E., Li, B., Payne, W.L., and Cebula, T.A. (1996) High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274: 1208-1211.
79. Li, X., and Lu, A.-L. (2001) Molecular cloning and functional analysis of the MutY homolog of Deinococcus radiodurans. J Bacteriol 183: 6151-6158.
80. Longerich, S., Galloway, A.M., Harris, R.S., Wong, C., and Rosenberg, S.M. (1995) Adaptive mutation sequences reproduced by mismatch repair deficiency. Proc Natl Acad Sci USA 92: 12017-12020.
81. McBeth, D.L., and Hauer, B. (1996) Increased mutagenesis mediated by cloned plasmid CAM-OCT genes: potential for expanding substrate ranges of Pseudomonas spp. Appl Environ Microbiol 62: 3538-3540.
82. McClintock, B. (1984) The significance of responses of the genome to challenge. Science 226: 792-801.
83. McKenzie, G.J., Lee, P.L., Lombardo, M.-J., Hastings, P.J., and Rosenberg, S.M. (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol Cell 7: 571-579.
84. Mahillon, J., and Chandler, M. (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
85. Maki, H., and Sekiguchi, M. (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355: 273-275.
86. Maloney, P.E., van Bruggen, A.H.C., and Hu, S. (1997) Bacterial community structure in relation to the carbon environments in lettuce and tomato rhizospheres and in bulk soil. Microb Ecol 34: 109-117.
87. Maor-Shoshani, A., and Livneh, Z. (2002) Analysis of the stimulation of DNA polymerase V of Escherichia coli by processivity proteins. Biochemistry 41: 14438-14446.
88. Marti, T.M., Kunz, C., and Fleck, O. (2002) DNA mismatch repair and mutation avoidance pathways. J Cell Physiol 191: 28-41.
89. Martinez, J.L., and Baquero, F. (2000) Mutation frequencies and antibiotic resistance. Antimicrob Agents Chemother 44: 1771-1777.
90. Mascher, F., Hase, C., Moënne-Loccoz, Y., and Défago, G. (2000) The viable-but-nonculturable state induced by antibiotic stress in the biocontrol agent Pseudomonas fluorescens CHA0 does not promote strain persistence in soil. Appl Environ Microbiol 66: 1662-1667.
91. Massey, R.C., and Buckling, A. (2002) Environmental regulation of mutation rates at specific sites. Trends Microbiol 10: 580-584.
92. Matic, I., Taddei, F., and Radman, M. (1996) Genetic barriers among bacteria. Trends Microbiol 4: 69-73.
93. Matic, I., Radman, M., Taddei, F., Picard, B., Doit, C., Bingen, E., et al. (1997) Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science 277: 1833-1834.
94. Metzgar, D., and Wills, C. (2000) Evidence for the adaptive evolution of mutation rates. Cell 101: 581-584.
95. Michaels, M.L., Cruz, C., Grollman, A.P., and Miller, J.H. (1992) Evidence that MutY and MutM combine to prevent mutations by an oxidatively damaged form of guanine in DNA. Proc Natl Acad Sci USA 89: 7022-7025.
96. Miller, J.H. (1998) Mutators in Escherichia coli. Mutat Res 409: 99-106.
97. Miller, J.H., Suthar, A., Tai, J., Yeung, A., Truong, C., and Stewart, J.L. (1999) Direct selection for mutators in Escherichia coli. J Bacteriol 181: 1576-1584.
98. Mittler, J.E., and Lenski, R.E. (1990) Excisions of Mu from E. coli MCS2 are not directed mutations. Nature 344: 173-175.
99. Moxon, E.R., Rainey, P.B., Nowak, M.A., and Lenski, R.E. (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24-33.
100. Naas, T., Blot, M., Fitch, W.M., and Arber, W. (1994) Insertion sequence-related genetic variation in resting Escherichia coli K-12. Genetics 136: 721-730.
101. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R.P.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV and Pol V) are involved in induced mutagenesis. EMBO J 19: 6259-6265.
102. Negishi, K., Loakes, D., and Schaaper, R.M. (2002) Saturation of DNA mismatch repair and error catastrophe by a base analogue in Escherichia coli. Genetics 161: 1363-1371.
103. Nghiem, Y., Cabrera, M., Cupples, C.G., and Miller, J.H. (1988) The mutY gene: a mutator locus in Escherichia coli that generates G:C-T:A transversions. Proc Natl Acad Sci USA 85: 2709-2713.
104. Notley-McRobb, L., Pinto, R., Seeto, S., and Ferenci, T. (2002a) Regulation of mutY and nature of mutator mutations in Escherichia coli populations under nutrient limitation. J Bacteriol 184: 739-745.
105. Notley-McRobb, L., Seeto, S., and Ferenci, T. (2002b) Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162: 1055-1062.
106. Ochman, H., Lawrence, J.G., and Groisman, E.A. (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
107. Oliver, A., Cantón, R., Campo, P., Baquero, F., and Blázquez, J. (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288; 1251-1253.
108. Oliver, A., Sánchez, J.M., and Blázquez, J. (2002) Characterization of the GO system of Pseudomonas aeruginosa. FEMS Microbiol Lett 217: 31-35.
109. van Overbeek, L.S., Eberl, L., Giskov, M., Molin, S., and van Elsas, J.D. (1995) Survival of, and induced stress resistance in, carbon-starved Pseudomonas fluorescens cells residing in soil. Appl Environ Microbiol 61: 4202-4208.
110. Papavasiliou, F.N., and Schatz, D.G. (2002) Somatic hypermutation of immunoglobulin genes: merging mechanisms for genetic diversity. Cell 109: S35-S44.
111. Pavlov, Y.I., Rogozin, I.B., Galkin, A.P., Aksenova, A.Y., Hanaoka, F., Rada, C., and Kunkel, T.A. (2002) Correlation of somatic hypermutation specificity and A-T base pair substitution errors by DNA polymerase η during copying of a mouse immunoglobulin κ light chain transgene. Proc Natl Acad Sci USA 99: 9954-9959.
112. Permina, E.A., Mironov, A.A., and Gelfand, M.S. (2002) Damage-repair error-prone polymerases of eubacteria: association with mobile genome elements. Gene 293: 133-140.
113. Petersen-Mahrt, S.K., Harris, R.S., and Neuberger, M.S. (2002) AID mutates E. coli suggesting a DNA deamination mechanism for antibody diversification. Nature 418: 99-103.
114. Poltoratsky, V., Woo, C.J., Tippin, B., Martin, A., Goodman, M.F., and Scharff, M.D. (2001) Expression of error-prone polymerases in BL2 cells activated for Ig somatic hypermutation. Proc Natl Acad Sci USA 98: 7976-7981.
115. Prival, M.J., and Cebula, T.A. (1992) Sequence analysis of mutations arising during prolonged starvation of Salmonella typhimurium. Genetics 132: 303-310.
116. Rada, C., Williams, G.T., Nilsen, H., Barnes, D.E., Lindahl, T., and Neuberger, M.S. (2002) Immunoglobulin isotype switching is inhibited and somatic hypermutation perturbed in UNG-deficient mice. Curr Biol 12: 1748-1755.
117. Radicella, J.P., Park, P.U., and Fox, M.S. (1995) Adaptive mutation in Escherichia coli: a role of conjugation. Science 268: 418-420.
118. Radman, M. (1999) Enzymes of evolutionary change. Nature 401: 866-869.
119. Radman, M., Taddei, F., and Matic, I. (2000) Evolution-driving genes. Res Microbiol 151: 91-95.
120. Rainey, P.B., and Travisano, M. (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69-72.
121. Ramos, C., Mølbak, L., and Molin, S. (2000) Bacterial activity in the rhizosphere analyzed at the single-cell level by monitoring ribosome contents and synthesis rates. Appl Environ Microbiol 66: 801-809.
122. Rattray, E.A.S., Prosser, J.I., Glover, L.A., and Killham, K. (1995) Characterization of rhizosphere colonization by luminescent Enterobacter cloacae at the population and single-cell levels. Appl Environ Microbiol 61: 2950-2957.
123. Rayssiguier, C., Thaler, D.S., and Radman, M. (1989) The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342: 396-401.
124. Richardson, A.R., Yu, Z., Popovic, T., and Stojilkovic, I. (2002) Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. Proc Natl Acad Sci USA 99: 6103-6107.
125. Rocha, E.P.C., Matic, I., and Taddei, F. (2002) Overrepresentation of repeats in stress response genes: a strategy to increase versatility under stressful conditions? Nucleic Acids Res 30: 1886-1894.
126. Rosenberg, S.M. (2001) Evolving responsively: adaptive mutation. Nature Rev Genet 2: 504-515.
127. Rosenberg, S.M., Longerich, S., Gee, P., and Harris, R.S. (1994) Adaptive mutation by deletions in small mononucleotide repeats. Science 265: 405-407
128. Rosenberg, S.M., Harris, R.S., Longerich, S., and Galloway, A.M. (1996) Recombination-dependent mutation in non-dividing cells. Mutat Res 350: 69-66
129. Sarand, I., Skärfstad, E., Forsman, M., Romantschuk, M., and Shingler, V. (2001) Role of the DmpR-mediated regulatory circuit in bacterial biodegradation properties in methylphenol-amended soils. Appl Environ Microbiol 67: 162-171.
130. Saumaa, S., Tover, A., Kasak, L., and Kivisaar, M. (2002) Different spectra of stationary-phase mutations in early-arising versus late-arising mutants of Pseudomonas putida: involvement of the DNA repair enzyme MutY and stationary-phase sigma factor RpoS. J Bacteriol 184: 6957-6965.
131. Schaaper, R.M., and Radman, M. (1989) The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J 8: 3511-3516.
132. Shapiro, J.A. (1997) Genome organization, natural genetic engineering and adaptive mutation. Trends Genet 13: 98-104.
133. Shapiro, J.A., and Higgins, N.P. (1989) Differential activity of a transposable element in Escherichia coli colonies. J Bacteriol 171: 5975-5986.
134. Shibutani, S., Takeshita, M., and Grollman, A.P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxoG. Nature 349: 431-434.
135. Sinha, H., Pain, A., and Johnstone, K. (2000) Analysis of the role of recA in phenotypic switching of Pseudomonas tolaasii. J Bacteriol 182: 6532-6535.
136. Sniegowski, P.D., Gerrish, P.J., and Lenski, R.E. (1997) Evolution of high mutation rates in experimental populations of E. coli. Nature 387: 703-705.
137. Söderberg, K.H., and Bååth, E. (1998) Bacterial activity along a young barley root measured by the thymidine and leucine incorporation techniques. Soil Biol Biochem 30: 1259-1268.
138. Štambuk, S., and Radman, M. (1998) Mechanism and control of interspecies recombination in Escherichia coli. I. Mismatch repair, methylation, recombination and replication functions. Genetics 150: 533-542.
139. Sternberg, C., Christensen, B.B., Johansen, T., Nielsen, A.T., Andersen, J.B., Giskov, M., and Molin, S. (1999) Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol 65: 4108-4117.
140. Strauss, B.S. (1992) The origin of mutations in human tumor cells. Cancer Res 52: 249-253.
141. Strauss, B.S. (1998) Hypermutability in carcinogenesis. Genetics 148: 1619-1626.
142. Su, S.-S., and Modrich, P. (1986) Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci USA 83: 5057-5061.
143. Sundin, G.W., Kidambi, S.P., Ullrich, M., and Bender, C.L. (1996) Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes. Gene 177: 77-81.
144. Sung, H.-M., and Yasbin, R.E. (2002) Adaptive, or stationary-phase, mutagenesis, a component of bacterial differentiation in Bacillus subtilis. J Bacteriol 184: 5641-5653.
145. Sutton, M.D., and Walker, G.C. (2001) Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination. Proc Natl Acad Sci USA 98: 8342-8349.
146. de Visser, J.A.G.M., Zeyl, C.W., Gerrish, P.J., Blanchard, J.L., and Lenski, R.E. (1999) Diminishing returns from mutation supply rate in asexual populations. Science 283: 404-406.
147. Taddei, F., Matic, I., and Radman, M. (1995) cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc Natl Acad Sci USA 92: 11736-11740.
148. Taddei, F., Radman, M., Maynard-Smith, J., Toupance, B., Gouyon, P.H., and Godelle, B. (1997) Role of mutator alleles in adaptive evolution. Nature 387: 700-702.
149. Tang, M., Pham, P., Shen, X., Taylor, J.-S., O'Donnell, M., Woodgate, R., and Goodman, M.F. (2000) Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature 404: 1014-1018.
150. Tenaillon, O., Toupance, B., Le Nagard, H., Taddei, F., and Godelle, B. (1999) Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics 152: 485-493.
151. Tenaillon, O., Taddei, F., Radman, M., and Matic, I. (2001) Second-order selection in bacterial evolution: selection acting on mutation and recombination rates in the course of adaptation. Res Microbiol 152: 11-16.
152. Thomas, A.W., Lewington, J., Hope, S., Topping, A.W., Weightman, A.J., and Slater, J.H. (1992) Environmentally directed mutations in the dehalogenase system of Pseudomonas putida strain PP3. Arch Microbiol 158: 176-182.
153. Timms, A.R., Muriel, W., and Bridges, B.A. (1999) UmuD, C-dependent pathway for spontaneous G: C to C: G transversions in stationary phase Escherichia coli mutY. Mutat Res 434: 77-80.
154. Torkelson, J., Harris, R.S., Lombardo, M.-J., Nagendran, J., Thulin, C., and Rosenberg, S.M. (1997) Genome-wide hypermutation in a subpopulation of stationary-phase cells underlies recombination-dependent adaptive mutation. EMBO J 16: 3303-3311.
155. Turner, K., Porter, J., Pickup, R., and Edwards, C. (2000) Changes in viability and macromolecular content of long-term batch cultures of Salmonella typhimurium measured by flow cytometry. J Appl Microbiol 89: 90-99.
156. van Veen, J.A., van Overbeek, L.S., and van Elsas, J.D. (1997) Fate and activity of microorganisms introduced into soil. Microbiol Mol Biol Rev 61: 121-135.
157. Wagner, J., and Nohmi, T. (2000) Escherichia coli DNA polymerase IV mutator activity: genetic requirements and mutational specificity. J Bacteriol 182: 4587-4595.
158. Wagner, J., Fujii, S., Gruz, P., Nohmi, T., and Fuchs, R.P. (2000) The β clamp targets DNA polymerase IV to DNA and strongly increases its processivity. EMBO Rep 1: 484-488.
159. Woodgate, R., and Sedgwick, S.G. (1992) Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues. Mol Microbiol 6: 2213-2218.
160. Yeiser, B., Pepper, E.D., Goodman, M.F., and Finkel, S.E. (2002) SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. Proc Natl Acad Sci USA 99: 8737-8741.
161. Zambrano, M.M., Siegele, D.A., Almiron, M., Tormo, A., and Kolter, R. (1993) Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259: 1757-1760.
162. Zeng, X., Winter, D.B., Kasmer, C., Kraemer, K.H., Lehmann, A.R., and Gearhart, P.J. (2001) DNA polymerase η is an A-T mutator in somatic hypermutation of immunoglobulin variable genes. Nature Immunol 2: 537-541.