Stress-induced mutagenesis and complex adaptation

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1792, 2014, Pages

  Ram, Yoav ^a   Hadany, Lilach ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Adaptive peak shifts; Evolvability; Mathematical model; Mutation rate; Stress induced variation; Trade off

Indexed keywords

ADAPTATION; FITNESS; MUTATION; NATURAL SELECTION; NUMERICAL MODEL; TRADE-OFF;

ADAPTATION; BIOLOGICAL MODEL; GENETICS; MUTAGENESIS; MUTATION RATE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTIVE FITNESS;

ADAPTATION, PHYSIOLOGICAL; GENETIC FITNESS; MODELS, GENETIC; MUTAGENESIS; MUTATION RATE; STRESS, PHYSIOLOGICAL;

EID: 85006284588     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.1025     Document Type: Article

References (92)

1. Sniegowski PD, Gerrish PJ, Johnson T, Shaver A. 2000 The evolution of mutation rates: separating causes from consequences. BioEssays22, 1057-1066. (doi: 10. 1002/1521-1878(200012) 22: 12, 1057:: AID-BIES3. 3. 0. CO; 2-W)
2. Denamur E, Matic I. 2006 Evolution of mutation rates in bacteria. Mol. Microbiol. 60, 820-827. (doi: 10. 1111/j. 1365-2958. 2006. 05150. x)
3. De Visser JAGM. 2002 The fate of microbial mutators. Microbiology148, 1247-1252.
4. Funchain P, Yeung A, Stewart JL, Lin R, Slupska MM, Miller JH. 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.
5. Montanari S et al. 2007 Biological cost of hypermutation in Pseudomonas aeruginosa strains from patients with cystic fibrosis. Microbiology 153, 1445-1454. (doi: 10. 1099/mic. 0. 2006/ 003400-0)
6. Kimura M. 1967 On the evolutionary adjustment of spontaneous mutation rates. Genet. Res. 9, 23-34. (doi: 10. 1017/S0016672300010284)
7. Liberman U, Feldman MW. 1986 Modifiers of mutation rate: a general reduction principle. Theor. Popul. Biol. 30, 125-142. (doi: 10. 1016/0040-5809 (86)90028-6)
8. Giraud A, Radman M, Matic I, Taddei F. 2001 The rise and fall of mutator bacteria. Curr. Opin. Microbiol. 4, 582-585. (doi: 10. 1016/S1369-5274(00)00254-X)
9. Sniegowski PD, Gerrish PJ, Lenski RE. 1997 Evolution of high mutation rates in experimental populations ofE. coli. Nature387, 703-705. (doi: 10. 1038/42701)
10. Wielgoss Set al. 2012 Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proc. Natl. Acad. Sci. USA110, 222-227. (doi: 10. 1073/pnas. 121957 4110)
11. Taddei F, Radman M, Maynard Smith J, Toupance B, Gouyon P-H, Godelle B. 1997 Role of mutator alleles in adaptive evolution. Nature387, 700-702. (doi: 10. 1038/42696)
12. Kessler D, Levine H. 1998 Mutator dynamics on a smooth evolutionary landscape. Phys. Rev. Lett. 80, 2012-2015. (doi: 10. 1103/PhysRevLett. 80. 2012)
13. Tenaillon O, Toupance B, Le Nagard H, Taddei F, Godelle B. 1999 Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics152, 485-493.
14. Leigh EGJ. 1970 Natural selection and mutability. Am. Nat. 104, 301-305. (doi: 10. 1086/282663)
15. 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. (doi: 10. 1080/10409230701648502)
16. Foster PL. 2007 Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42, 373-397. (doi: 10. 1080/10409230701648494)
17. Rosenberg SM, Shee C, Frisch RL, Hastings PJ. 2012 Stress-induced mutation via DNA breaks in Escherichia coli: a molecular mechanism with implications for evolution and medicine. BioEssays 34, 885-892. (doi: 10. 1002/bies. 201200050)
18. Bjedov I, Tenaillon O, Gérard B, Souza V, Denamur E, Radman M, Taddei F, Matic I. 2003 Stress-induced mutagenesis in bacteria. Science 300, 1404-1409. (doi: 10. 1126/science. 1082240)
19. Katz S, Hershberg R. 2013 Elevated mutagenesis does not explain the increased frequency of antibiotic resistant mutants in starved aging colonies. PLoS Genet. 9, e1003968. (doi: 10. 1371/ journal. pgen. 1003968)
20. Kivisaar M. 2010 Mechanisms of stationary-phase mutagenesis in bacteria: mutational processes in pseudomonads. FEMS Microbiol. Lett. 312, 1-14. (doi: 10. 1111/j. 1574-6968. 2010. 02027. x)
21. Kang JM, Iovine NM, Blaser MJ. 2006 A paradigm for direct stress-induced mutation in prokaryotes. FASEB J. 20, 2476-2485. (doi: 10. 1096/fj. 06-6209com)
22. Baharoglu Z, Mazel D. 2011 Vibrio choleraetriggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob. Agents Chemother. 55, 2438-2441. (doi: 10. 1128/AAC. 01549-10)
23. Henderson-BeggSK, LivermoreDM, HallLMC. 2006 Effect of subinhibitory concentrations of antibiotics on mutation frequency inStreptococcus pneumoniae. J. Antimicrob. Chemother. 57, 849-854. (doi: 10. 1093/ jac/dkl064)
24. Heidenreich E. 2007 Adaptive mutation in Saccharomyces cerevisiae. Crit. Rev. Biochem. Mol. Biol. 42, 285-311. (doi: 10. 1080/104092307015 07773)
25. Rodriguez GP, Romanova NV, Bao G, Rouf NC, Kow YW, Crouse GF. 2012 Mismatch repair-dependent mutagenesis in nondividing cells. Proc. Natl Acad. Sci. USA109, 6153-6158. (doi: 10. 1073/pnas. 1115361109)
26. Goho S, Bell G. 2000 Mild environmental stress elicits mutations affecting fitness inChlamydomonas. Proc. R. Soc. Lond. B267, 123-129. (doi: 10. 1098/ rspb. 2000. 0976)
27. Matsuba C, Ostrow DG, Salomon MP, Tolani A, Baer CF. 2012 Temperature, stress and spontaneous mutation inCaenorhabditis briggsaeand Caenorhabditis elegans. Biol. Lett. 9, 20120334. (doi: 10. 1098/rsbl. 2012. 0334)
28. Sharp NP, Agrawal AF. 2012 Evidence for elevated mutation rates in low-quality genotypes. Proc. Natl Acad. Sci. USA109, 6142-6146. (doi: 10. 1073/pnas. 1118918109)
29. Bristow RG, Hill RP. 2008 Hypoxia and metabolism: hypoxia, DNA repair and genetic instability. Nat. Rev. Cancer8, 180-192. (doi: 10. 1038/nrc2344)
30. 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. Cell19, 791-804. (doi: 10. 1016/j. molcel. 2005. 07. 025)
31. Debora BN, Vidales LE, Ramírez R, Ramírez M, Robleto EA, Yasbin RE, Pedraza-Reyes M. 2010 Mismatch repair modulation of MutY activity drivesBacillus subtilis stationary-phase mutagenesis. J. Bacteriol. 193, 236-245. (doi: 10. 1128/JB. 00940-10)
32. Al Mamun AAMet al. 2012 Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 338, 1344-1348. (doi: 10. 1126/science. 1226683)
33. Tenaillon O, Denamur E, Matic I. 2004 Evolutionary significance of stress-induced mutagenesis in bacteria. Trends Microbiol. 12, 264-270. (doi: 10. 1016/j. tim. 2004. 04. 002)
34. Cirz RT, Romesberg FE. 2007 Controlling mutation: intervening in evolution as a therapeutic strategy. Crit. Rev. Biochem. Mol. Biol. 42, 341-354. (doi: 10. 1080/10409230701597741)
35. Agrawal AF. 2002 Genetic loads under fitnessdependent mutation rates. J. Evol. Biol. 15, 1004-1010. (doi: 10. 1046/j. 1420-9101. 2002. 00464. x)
36. Shaw FH, Baer CF. 2011 Fitness-dependent mutation rates in finite populations. J. Evol. Biol. 24, 1677-1684. (doi: 10. 1111/j. 1420-9101. 2011. 02320. x)
37. Ram Y, Hadany L. 2012 The evolution of stressinduced hypermutation in asexual populations. Evolution66, 2315-2328. (doi: 10. 1111/j. 1558-5646. 2012. 01576. x)
38. Wright S. 1931 Evolution in Mendelian populations. Genetics16, 97-159.
39. Wright S. 1988 Surfaces of selective value revisited. Am. Nat. 131, 115-123. (doi: 10. 1086/284777)
40. Crow JF, Engels WR, Denniston C. 1990 Phase three of Wright's shifting-balance theory. Evolution44, 233. (doi: 10. 2307/2409403)
41. Wade MJ, Goodnight CJ. 1991 Wright's shifting balance theory: an experimental study. Science253, 1015-1018. (doi: 10. 1126/science. 1887214)
42. Peck SL, Ellner SP, Gould F. 2000 Varying migration and deme size and the feasibility of the shifting balance. Evolution54, 324-327. (doi: 10. 1111/j. 0014-3820. 2000. tb00035. x)
43. Moore FB-G, Tonsor SJ. 1994 A simulation of Wright's shifting-balance process: migration and the three phases. Evolution48, 69-80. (doi: 10. 2307/ 2410004)
44. Gavrilets S. 1996 On phase three of the shiftingbalance theory. Evolution50, 1034-1041. (doi: 10. 2307/2410644)
45. Coyne JA, Barton NH, Turelli M. 2000 Is Wright's shifting balance process important in evolution? Evolution54, 306-317. (doi: 10. 1111/j. 0014-3820. 2000. tb00033. x)
46. Whitlock MC, Phillips PC. 2000 The exquisite corpse: a shifting view of the shifting balance. Trends Ecol. Evol. 15, 347-348. (doi: 10. 1016/S0169-5347(00) 01930-3)
47. Whitlock MC. 1995 Variance-induced peak shifts. Evolution49, 252-259. (doi: 10. 2307/2410335)
48. Whitlock MC. 1997 Founder effects and peak shifts without genetic drift: adaptive peak shifts occur easily when environments fluctuate slightly. Evolution51, 1044-1048. (doi: 10. 2307/2411033)
49. Hadany L. 2003 Adaptive peak shifts in a heterogenous environment. Theor. Popul. Biol. 63, 41-51. (doi: 10. 1016/S0040-5809(02)00011-4)
50. Hadany L, Beker T. 2003 Fitness-associated recombination on rugged adaptive landscapes. J. Evol. Biol. 16, 862-870. (doi: 10. 1046/j. 1420-9101. 2003. 00586. x)
51. Weissman DB, Desai MM, Fisher DS, Feldman MW. 2009 The rate at which asexual populations cross fitness valleys. Theor. Popul. Biol. 75, 286-300. (doi: 10. 1016/j. tpb. 2009. 02. 006)
52. Weissman DB, Feldman MW, Fisher DS. 2010 The rate of fitness-valley crossing in sexual populations. Genetics186, 1389-1410. (doi: 10. 1534/genetics. 110. 123240)
53. Gibson JLet al. 2010 Thes E stress response is required for stress-induced mutation and amplification in Escherichia coli. Mol. Microbiol. 77, 415-430. (doi: 10. 1111/j. 1365-2958. 2010. 07213. x)
54. Haigh J. 1978 The accumulation of deleterious genes in a population: Muller's Ratchet. Theor. Popul. Biol. 14, 251-267. (doi: 10. 1016/0040-5809(78)90027-8)
55. Gessler DDG. 1995 The constraints of finite size in asexual populations and the rate of the ratchet. Genet. Res. 66, 241. (doi: 10. 1017/S00166723000 34686)
56. Gordo I, Dionisio F. 2005 Nonequilibrium model for estimating parameters of deleterious mutations. Phys. Rev. E71, 18-21. (doi: 10. 1103/PhysRevE. 71. 031907)
57. Kibota TT, Lynch M. 1996 Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature381, 694-696. (doi: 10. 1038/ 381694a0)
58. Gordo I, Perfeito L, Sousa A. 2011 Fitness effects of mutations in bacteria. J. Mol. Microbiol. Biotechnol. 21, 20-35. (doi: 10. 1159/000332747)
59. Drake JW, Charlesworth B, Charlesworth D, Crow JF. 1998 Rates of spontaneous mutation. Genetics148, 1667-1686.
60. Wielgoss S, Barrick JE, Tenaillon O, Cruveiller S, Chane-Woon-Ming B, Médigue C, Lenski RE, Schneider D. 2011 Mutation rate inferred from synonymous substitutions in a long-term evolution experiment withEscherichia coli. Genes Genome Genet. 1, 183-186. (doi: 10. 1534/g3. 111. 000406)
61. Hall LMC, Henderson-Begg SK. 2006 Hypermutable bacteria isolated from humans: a critical analysis. Microbiology152, 2505-2514. (doi: 10. 1099/mic. 0. 29079-0)
62. Pupo GM, Richardson BJ. 1995 Biochemical genetics of a natural population ofEscherichia coli: seasonal changes in alleles and haplotypes. Microbiology 141, 1037-1044. (doi: 10. 1099/13500872-141-4-1037)
63. Berg OG. 1996 Selection intensity for codon bias and the effective population size ofEscherichia coli. Genetics142, 1379-1382.
64. Eshel I. 1981 On the survival probability of a slightly advantageous mutant gene with a general distribution of progeny size: a branching process model. J. Math. Biol. 12, 355-362. (doi: 10. 1007/ BF00276922)
65. Fisher RA. 1930 The genetical theory of natural selection. Oxford, UK: Clarendon Press.
66. Patwa Z, Wahl LM. 2008 The fixation probability of beneficial mutations. J. R. Soc. Interface 5, 1279-1289. (doi: 10. 1098/rsif. 2008. 0248)
67. Weinreich DM, Chao L. 2005 Rapid evolutionary escape by large populations from local fitness peaks is likely in nature. Evolution59, 1175-1182. (doi: 10. 1111/j. 0014-3820. 2005. tb01769. x)
68. Maynard Smith J, Haigh J. 1974 The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23-35. (doi: 10. 1017/S0016672300014634)
69. Lynch M, Bürger R, Butcher D, Gabriel W. 1993 The mutational meltdown in asexual populations. J. Hered. 84, 339-344.
70. Obolski U, Hadany L. 2012 Implications of stressinduced genetic variation for minimizing multidrug resistance in bacteria. BMC Med. 10, 1-30. (doi: 10. 1186/1741-7015-10-89)
71. Shor E, Fox CA, Broach JR. 2013 The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress. PLoS Genet. 9, e1003680. (doi: 10. 1371/journal. pgen. 1003680)
72. Karpinets T, Greenwood D, Pogribny I, Samatova N. 2006 Bacterial stationary-state mutagenesis and mammalian tumorigenesis as stress-induced cellular adaptations and the role of epigenetics. Curr. Genomics7, 481-496. (doi: 10. 2174/138920206 779315764)
73. Torres-Barceló C, Cabot G, Oliver A, Buckling A, MacLean RC. 2013 A trade-off between oxidative stress resistance and DNA repair plays a role in the evolution of elevated mutation rates in bacteria. Proc. R. Soc. B280, 20130007. (doi: 10. 1098/rspb. 2013. 0007)
74. Dawson KJ. 1998 Evolutionarily stable mutation rates. J. Theor. Biol. 194, 143-157. (doi: 10. 1006/ jtbi. 1998. 0752)
75. Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F. 2001 Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science291, 2606-2608. (doi: 10. 1126/ science. 1056421)
76. Loh E, Salk JJ, Loeb LA. 2010 Optimization of DNA polymerase mutation rates during bacterial evolution. Proc. Natl Acad. Sci. USA107, 1154-1159. (doi: 10. 1073/pnas. 0912451107)
77. Gentile CF, Yu S-C, Serrano SA, Gerrish PJ, Sniegowski PD. 2011 Competition between highand higher-mutating strains ofEscherichia coli. Biol. Lett. 7, 422-424. (doi: 10. 1098/rsbl. 2010. 1036)
78. Shee C, Gibson JL, Darrow MC, Gonzalez C, Rosenberg SM. 2011 Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation inEscherichia coli. Proc. Natl Acad. Sci. USA108, 13 659-13 664. (doi: 10. 1073/pnas. 1104681108)
79. Tenaillon O, Le Nagard H, Godelle B, Taddei F. 2000 Mutators and sex in bacteria: conflict between adaptive strategies. Proc. Natl Acad. Sci. USA97, 10 465-10 470. (doi: 10. 1073/pnas. 180063397)
80. Johnson T, Barton NH. 2002 The effect of deleterious alleles on adaptation in asexual populations. Genetics162, 395-411.
81. Leigh EGJ. 1973 The evolution of mutation rates. Genetics73(Suppl. 73), 1-18.
82. Komarova NL, Wodarz D. 2004 The optimal rate of chromosome loss for the inactivation of tumor suppressor genes in cancer. Proc. Natl Acad. Sci. USA 101, 7017-7021. (doi: 10. 1073/pnas. 0401943101)
83. Komarova NL, Sadovsky AV, Wan FYM. 2008 Selective pressures for and against genetic instability in cancer: a time-dependent problem. J. R. Soc. Interface 5, 105-121. (doi: 10. 1098/rsif. 2007. 1054)
84. Agur Z, Mazor G, Meilijson I. 1991 Maturation of the humoral immune response as an optimization problem. Proc. R. Soc. Lond. B245, 147-150. (doi: 10. 1098/rspb. 1991. 0101)
85. Jackson AL, Loeb LA. 1998 The mutation rate and cancer. Genetics148, 1483-1490.
86. Bielas JH, Loeb KR, Rubin BP, True LD, Loeb LA. 2006 Human cancers express a mutator phenotype. Proc. Natl Acad. Sci. USA103, 18 238-18 242. (doi: 10. 1073/pnas. 0607057103)
87. Lambert G, Estévez-Salmeron L, Oh S, Liao D, Emerson BM, Tlsty TD, Austin RH. 2011 An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat. Rev. Cancer11, 375-382. (doi: 10. 1038/nrc3039)
88. Ruan K, Song G, Ouyang G. 2009 Role of hypoxia in the hallmarks of human cancer. J. Cell. Biochem. 107, 1053-1062. (doi: 10. 1002/jcb. 22214)
89. Bindra RS, Crosby ME, Glazer PM. 2007 Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev. 26, 249-260. (doi: 10. 1007/s10555-007-9061-3)
90. Podlaha O, Riester M, De S, Michor F. 2012 Evolution of the cancer genome. Trends Genet. 28, 155-163. (doi: 10. 1016/j. tig. 2012. 01. 003)
91. Schrag SJ, Perrot V, Levin BR. 1997 Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc. R. Soc. Lond. B264, 1287-1291. (doi: 10. 1098/ rspb. 1997. 0178)
92. Perez F, Granger BE. 2007 IPython: a system for interactive scientific computing. Comput. Sci. Eng. 9, 21-29. (doi: 10. 1109/MCSE. 2007. 53)