Mutators and hypermutability in bacteria: The Escherichia coli paradigm

Journal of Genetics

Volumn 88, Issue 3, 2010, Pages 379-391

  Jayaraman, R ^a,b  

^a Madurai Kamaraj University ^*  (India)

^b MADURAI KAMARAJ UNIVERSITY   (India)

Author keywords

Causes of hypermutability; Escherichia coli; Hypermutators; Mutators

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA;

DNA DAMAGE; DNA REPLICATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM; MISMATCH REPAIR; MUTATION; REVIEW;

DNA DAMAGE; DNA MISMATCH REPAIR; DNA POLYMERASE III; DNA REPLICATION; ESCHERICHIA COLI; MUTATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 73949101830     PISSN: 00221333     EISSN: 09737731     Source Type: Journal    
DOI: 10.1007/s12041-009-0058-2     Document Type: Review

References (116)

1. Al Mamun A. A. 2007 Elevated expression of DNA polymerase II increases spontaneous mutagenesis in Escherichia coli. Mutat. Res. 625, 29-39.
2. Al Mamun A. A., Gautam S. and Humayun M. Z. 2006 Hypermutagenesis in mutA cells is mediated by mistranslational corruption of polymerase, and is accompanied by replication fork collapse. Mol. Microbiol. 62, 1752-1763.
3. Balashov S. and Humayun M. Z. 2003 Escherichia coli cells bearing a ribosomal ambiguity mutation in rpsD have a mutator phenotype that correlates with increased mistranslation. J. Bacteriol. 185, 5015-5018.
4. Bennett S. E., Chen C. and Mosbaugh D. W. 2004 Escherichia coli nucleoside kinase does not act as a uracil processing DNA repair nuclease. Proc. Natl. Acad. Sci. USA101, 6391-6396.
5. Bessman M. J., Frick D. N. and O'Handley S. F. 1996 The mutT proteins or "nudix hydrolase", a family of versatile, widely distributed "house-keeping" enzymes. J. Biol. Chem. 271, 25059-25062.
6. Bjelland S. and Seaberg E. 2003 Mutagenecity, toxicity and repair of DNA base damage by oxidation. Mutat. Res. 531, 37-80.
7. Blazquez J. 2003 Hypermutation as a factor cotributing to the acquisition of antimicrobial resistance. Clin. Inf. Dis. 37, 1201-1209.
8. Branum M. E., Reardon J. T. and Sancar A. 2001 DNA repair excision nuclease attacks undamaged DNA: a source of spontaneous mutation. J. Biol. Chem. 276, 25421-25426.
9. Bridges B. A. 1996 Elevated mutation rate in mutT bacteria during starvation: evidence for DNA turnover? J. Bacteriol. 178, 2709-2711.
10. 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.
11. Carter J. R., Franden M. A., Aebersold R., Kim R. and Mc Henry C. S. 1993 Isolation, sequencing and over expression of the gene encoding the θ subunit of DNA polymerase III holoenzyme. Nucleic Acids Res. 21, 3261-3286.
12. Chikova A. K. and Schaaper R. M. 2005 The bacteriophage P1 hot gene product can substitute for the Escherichia coli DNA polymerase III subunit. J. Bacteriol. 187, 5528-5536.
13. Chikova A. K. and Schaaper R. M. 2006 Mutator and antimutator effects of the bacteriophage P1 hot gene product. J. Bacteriol. 188, 5831-5838.
14. Drake J. W. 1993 General antimutators and improbable. J. Mol. Biol. 229, 8-13.
15. Drake J. W., Allen E. F., Forsberg S. A., Prepatra R. M. and Greening E. O. 1969 Genetic control of mutation rates in bacteriophage T4. Nature221, 1128-1132.
16. David S. S., O'shea V. L. O. and Kundu S. 2007 Base excision repair of oxidative DNA damage. Nature447, 941-950.
17. Degnen G. E. and Cox E. C. 1974 Conditional mutator gene in Escherichia coli: isolation, mapping and effector studies. J. Bacteriol. 117, 477-487.
18. Denamur E., Lecointro G., Darlu P., Tenaillon O., Acquaviva C., Sayada C. et al. 2000 Evolutionary implications of the frequent horizontal transfer of mismatch repair genes. Cell103, 711-721.
19. Denamur E. and Matic I. 2006 Evolution of mutation rates in bacteria. Mol. Microbiol. 60, 820-827.
20. de Visser J. A. G. M. 2002 The fate of microbial mutators. Microbiology148, 1247-1252.
21. Di Francesco R., Bhatnagar S. K., Brown A. and Bessman M. J. 1984 The interaction of DNA polymerase III and the product of the Escherichia coli mutator gene mutD. J. Biol. Chem. 259, 5567-5573.
22. Echols H., Lu C. and Burgers P. M. J. 1983 Mutator strains of Escherichia coli, mutD and dnaQ, with defective exonucleolytic editing by DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. USA80, 2189-2192.
23. Fijalkowska I. J. and Schaaper R. M. 1993 Antimutator mutations in the alpha subunit of Escherichia coli DNA polymerase III: Identification of the responsible mutations and alignment with other DNA polymerases. Genetics134, 1039-1044.
24. Fijalkowska I. M. and Schaaper R. M. 1995 Effects of Escherichia coli dnaE antimutator alleles in a proof-reading defective mutD5 strain. J. Bacteriol. 177, 5979-5986.
25. Fijalkowska I. M. and Schaaper R. M. 1996 Mutants in the exoI motif of Escherichia coli dnaQ: defective proof-reading and inviability due to error catastrophe. Proc. Natl. Acad. Sci. USA93, 2856-2861.
26. Foster P. L. 2007 Stress induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42, 373-397.
27. Fowler R. G. and Schaaper R. M. 1997 The role of the mutT gene of Escherichia coli in maintaining replication fidelity. FEMS Microbiol. Rev. 21, 43-54.
28. Fowler R. G., White S. J., Kayama C., Moore S. C., Dunn R. L. and Schaaper R. M. 2003 Interaction among the Escherichia coli mutT, mutM and mutY damage prevention pathways. DNA Repair2, 159-173.
29. Friedberg E. C. 2006 The eureka enzyme: the discovery of DNA polymerase. Nat. Rev. Mol. Cell Biol. 7, 143-147.
30. Friedberg E. C., Walker G. C., Siede W., Wood R. D., Schultz R. A. and Ellenberger E. 2006 DNA repair and mutagenesis, 2nd edition. ASM Press, Washington DC, USA.
31. Fuchs R. D., Fujii S. and Wagner J. 2004 Properties and functions of Escherichia coli Pol IV and Pol V. Adv. Protein Chem. 69, 229-264.
32. Funchain P., Yeung A., Lee J., Lin R., Slupska M. M. and Miller J. H. 2000 The consequences of growth of a mutator strain of Escherichia coli by loss of function among multiple gene targets and loss of fitness. Genetics154, 959-970.
33. Funchain P., Yeung A., Stewart J., Clandenin W. M. and Miller J. H. 2001 Amplification of mutator cells in a population. J. Bacteriol. 183, 3737-3741.
34. Galhardo R. S., Hastings P. J. and Rosenberg S. M. 2007 Mutation as a stress response and the regulation of evolvability. Crit. Rev. Biochem. Mol. Biol. 42, 399-435.
35. Gawel D., Pham I., Fijalkowska I. M., Jonczyk P. and Schaaper R. M. 2008 Role of accessory DNA polymerases in DNA replication in Escherichia coli: analysis of the dnaX36 mutator mutant. J. Bacteriol. 190, 1730-1742.
36. Giraud A., Matic I., Tenaillon O., Clara A., Radman M., Fons M. et al. 2001 Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science291, 2606-2608.
37. Giraud A., Matic I., Radman M., Fons M. and Taddie F. 2002 Mutator bacteria as a risk factor in the treatment of infectious diseases. Antimicrob. Agents Chemother. 46, 863-865.
38. Gonsalez C., Hadany L., Ponder R. G., Price M., Hastings P. J. and Rosenberg S. M. 2008 Mutability and importance of a hypermutable cell sub-population that produces stress-induced mutations in Escherichia coli. PLoS. Genet. 4, e 1000208. doi10. 1371/journal. pgen. 1000208.
39. Goodman M. F. 2002 Error prone repair DNA polymerases in prokaryotes and eukaryotes. Annu. Rev. Biochem. 71, 17-50.
40. Gorini L. 1969 The contrasting role of strA and ram gene products in ribosomal functioning. Cold Spring Harbor Symp. Quant. Biol. 34, 101-111.
41. Goswami S. C., Yoon J-H., Abramczyk B. M., Pfiefer G. and Postel E. H. 2006 Molecular and functional interaction between Escherichia coli nucleoside diphosphate kinase and the uracil-DNA glycosylase. Ung. J. Biol. Chem. 281, 32131-32139.
42. Grollman A. P. and Moriya M. 1993 Mutagenesis by 8-oxo-guanine: the enemy within. Trends Genet. 9, 246-249.
43. Hastings P. J. 2007 Adaptive amplification. Crit. Rev. Biochem. Mol. Biol. 42, 271-283.
44. Hall M. C. and Henderson-Begg S. K. 2006 Hypermutable bacteria isolated from humans: a critical analysis. Microbiology152, 2505-2514.
45. Henson T. M., Chu H., Irwin C. A. and Walker J. R. 1979 Isolation and characterisation of dnaX and dnaY temperature sensitive mutants of Escherichia coli. Genetics92, 1041-1059.
46. Hasegawa K., Yoshiama K. and Maki H. 2008 Spontaneous mutagenesis associated with nucleotide excision repair in Escherichia coli. Genes Cells13, 459-469.
47. Herman G. E. and Modrich P. 1981 Escherichia coli K-12 clones that overproduce dam methylase are hypermutable. J. Bacteriol. 145, 644-646.
48. Horiuchi T., Maki H. and Sekiguchi M. 1978 A new conditonal lethal mutator (dnaQ49) in Escherichia coli K12. Mol. Gen. Genet. 163, 277-291.
49. Horst J-P., Wu T. and Marinus M. G. 1999 Escherichia coli mutator genes. Trends Microbiol. 7, 29-36.
50. Hong S. E., Yueng A., Funchain P., Slupska M. M. and Miller J. H. 2005 Mutants with temperature sensitive defects in the Eschericha coli mismatch repair system. J. Bacteriol. 187, 840-846.
51. Hsu G., Ober M., Carell T. and Besso L. S. 2004 Error prone replication of oxidatively damaged DNA by a high fidelity DNA polymerase. Nature431, 217-221.
52. Humayun M. Z. 1998 SOS and Mayday: multiple inducible mutagenic pathways in Escherichia coli. Mol. Microbiol. 30, 905-910.
53. Imlay J. A. 2003 Pathways of oxidative DNA damages. Annu. Rev. Microbiol. 57, 395-418.
54. Iyer R. R., Plucciennik A., Burdett V. and Modrich P. L. 2006 DNA mismatch repair: functions and mechanisms. Chem. Rev. 106, 302-323.
55. Jiricny J. 2006 The multifaceted mismatch repair system. Nat. Rev. Mol. Cell Biol. 7, 335-346.
56. Kuban W., Banach-Orlowska M., Bialoskorska M., Lipowska A., Schaaper R. M., Jonczyk P. et al. 2005 Mutator phenotype resulting from DNA polymerase IV over production in Escherichia coli: preferential mutagenesis in the lagging strand. J. Bacteriol. 187, 6852-6866.
57. Kuban W., Banach-Orlowska M., Schaaper R. M., Jonczyk P. and Fijalkowska I. J. 2006 Role of DNA polymerase IV in Escherichia coli mutator activity. J. Bacteriol. 188, 7977-7980.
58. Kumar P., Krishna K., Srinivasan R., Ajit Kumar P. and Varshney U. 2004 Mycobacterium tuberculosis and Escherichia coli nucleoside diphospho kinases lack multifunctional activities to process uracil containing DNA. DNA Repair3, 1483-1492.
59. Kunkel T. A. and Erie D. A. 2005 DNA mismatch repair. Annu. Rev. Biochem. 74, 681-710.
60. Lacombe M. L., Milon l., Munier A., Mehus J. G. and Lambeth D. O. 2000 The human NM23 / nucleotide diphosphokinases. J. Bioenerg. Biomembr. 32, 247-258.
61. LeClerc J. E., Payne W. L., Kupchella E. and Cebula T. A. 1996 High mutation frequencies among Escherichia coli and Salmonella pathogens. Science274, 1208-1211.
62. Lobner-Oleson A., Skovgaard O. and Marinus M. G. 2005 Dam methylation: coordinating cellular processes. Curr. Opin. Microbiol. 8, 154-160.
63. Lu Q., Zhang X., Almaula N., Mathews C. K. and Inoyue M. 1995 The gene for nucleoside diphosphate kinase is a mutator gene in Escherichia coli. J. Mol. Biol. 254, 337-341.
64. Lu Q. and Inouye M. 1996 Adenylate kinase complements nucleoside kinase deficiency in nucleotide metabolism. Proc. Natl. Acad. Sci. USA93, 5720-5725.
65. Macia M. D., Blanquer D., Togores B., Sauleda J., Perez J. L. and Oliver A. 2005 Hypermutation is a key factor in development of multiple antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob. Agents Chemother. 49, 3382-3386.
66. Maki H. 2002 Origin of spontaneous mutations: specificity and directionality of base substitution, frame shift and sequence substitution mutagenesis. Annu. Rev. Genet. 36, 279-303.
67. Maki H. and Kornberg A. 1987 Proof reading by DNA polymerase III of Escherichia coli depends upon cooperative interaction of the polymerase and exonuclease subunits. Proc. Natl. Acad. Sci. USA84, 4389-4392.
68. Maki H., Mo J. Y. and Sekiguchi M. 1991 A strong mutator effect caused by an aminoacid change in the a subunit of DNA polymerase III of Escherichia coli. J. Biol. Chem. 266, 5055-5061.
69. Marinus M. G. and Morris N. R. 1974 Biological function of 6-methyl adenine in the DNA of Escherichia coli. J. Mol. Biol. 85, 309-322.
70. Mathews C. K. 2006 DNA precursor metabolism and genomic stability. FASEB J. 20, 1300-1314.
71. Matic I. 2008 Biological role of Escherichia coli translesion DNA polymerase IV. Period. Biol. 110, 213-217.
72. Matic I., Radman M., Taddie F., Picard B., Doit C. and Binger E. 1997 Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science277, 1833-1834.
73. Mc Henry C. S. 2003 Chromosomal replicases as asymmetric dimers: Studies on subunit arrangements and functional consequences. Mol. Microbiol. 49, 1157-1165.
74. Michaels M. L., Cruz C. and Miller J. H. 1990 mutA and mutC, two mutator loci in Escherichia coli that stimulate transversions. Proc. Natl. Acad. Sci. USA87, 9211-9215.
75. Michaels M. L. and Miller J. H. 1992 The GO system prevents organisms from mutagenic effects of the spontaneous lesion 8-hydroxy guanine (7, 8-dihydro-8-oxo guanine). J. Bacteriol. 174, 6321-6325.
76. Miller J. 1996 Spontaneous mutators in bacteria: Insights into pathways of mutagenesis and repair. Annu. Rev. Microbiol. 50, 625-643.
77. Miller J. H., Suthar A., Tai J., Yeung A., Truong C. and Stewart J. L. 1999 Direct selection of mutators in Escherichia coli. J. Bacteriol. 181, 1576-1584.
78. Miller J. H., Funchain P., Clendenin W., Huang T., Nguyen A., Wolff E. et al. 2002 Escherichia coli strains (ndk) lacking nucleoside diphosphate kinase are powerful mutators for base substitutions and frame shifts in mismatch deficient strains. Genetics162, 5-13.
79. Mo J. Y., Maki H. and Sekiguchi M. 1991 Mutational specificity of the dnaE173 mutator associated with defects in the catalytic subunit of DNA polymerase III of Escherichia coli. J. Mol. Biol. 222, 925-993.
80. Muzycka N., Poland R. L. and Bessman M. J. 1972 Studies on the biochemical basis of spontaneous mutations. I. A comparison of DNA polymerases of antimutator, mutator and wild type strains of bacteriophage T4. J. Biol. Chem. 247, 7116-7122.
81. Nohmi T. 2006 Environmental stress and lesion by pass polymerases. Annu. Rev. Microbiol. 60, 231-253.
82. Nordman A., Skorgaard O. and Wright A. 2007 A novel class of mutations that affect DNA replication in Escherichia coli. Mol. Microbiol. 64, 125-138.
83. Nordman J. and Wright A. 2008 Relationship between NTP pool levels and mutagenesis in an Escherichia coli NDP-kinase mutant. Proc. Natl. Acad. Sci. USA105, 10195-10202.
84. Nowosielska A., Janion C. and Grzesiuk E. 2004 Effect of deletion of SOS- induced polymerases pol II, pol IV and pol V on spontaneous mutagenesis in Escherichia coli mutD5. Environ. Mol. Mutagen. 43, 226-234.
85. O'Donnell M. 2006 Replisome architecture and dynamics in Escherichia coli. J. Biol. Chem. 281, 10653-10656.
86. Oliver A. 2005 Hypermutation in natural bacterial population: consequences for medical microbiology. Rev. Med. Microbiol. 16, 1-25.
87. Oliver A., Canton R., Campo P., Bacquero F. and Blazquez J. 2000 High frequency of hypermutable Psedomonas aeruginosa in cytic fibrosis lung infection. Science288, 1251-1254.
88. Pal C., Macia M. D., Oliver A., Schachar I. and Buckling A. 2007 Co-evolution with viruses drives the evolution of bacterial mutation rates. Nature450, 1079-1081.
89. Petit M. A., Dinpft J., Radman M. and Echols H. 1991 Control of large chromosomal duplications in Escherichia coli by the mismatch repair system. Genetics129, 327-332.
90. Pham P. T., Zhao W. and Schaaper R. M. 2006 Mutator mutants of Escherichia coli carrying a defect in the DNA polymerase τ subunit. Mol. Microbiol. 59, 1149-1161.
91. Postel E. H. and Abramczyk B. M. 2003 Escherichia coli nucleoside diphosphate kinase is a uracil-processing DNA repair nuclease. Proc. Natl. Acad. Sci. USA100, 13247-13252.
92. Radman M., Matic I. and Taddie F. 1999 Evolution of evolvability. Ann. N. Y. Acad. Sci. 847, 146-155.
93. Rayssiguier C., Thaler D. and Radman M. 1989 The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch repair mutants. Nature342, 396-401.
94. Roth J. R., Kugelberg E., Reams A. B., Kofoid A. B. and Andersson D. I. 2005 Origin of mutation under selection: the adaptive mutation controversy. Annu. Rev. Microbiol. 60, 477-501.
95. Schaaper R. M. 1998 Antimutator mutants of bacteriophage T4 and Escherichia coli. Genetics148, 1579-1585.
96. Scheurmann R. and Echols H. 1984 A separate editing exonuclease for DNA replication: the subunit of Escherichia coli DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. USA81, 7747-7751.
97. Scheurmann R., Tam S., Burgers P. M. J., Lu C. and Echols H. 1983 Identification of the ∈ subunit of DNA polymease III holoenzyme as the dnaQ gene product: A fidelity subunit of DNA replication. Proc. Natl. Acad. Sci. USA80, 7085-7089.
98. Schlacher K., Pham T., Cox M. M. and Goodman M. F. 2006 Roles of DNA polymerase V and RecA protein in SOS induced mutation. Chem. Rev. 106, 406-419.
99. Schofield M. J. and Hsieh P. 2003 Mismatch repair: molecular mechanisms and biological functions. Annu. Rev. Microbiol. 57, 579-608.
100. Shibutani S., Takeshita M. and Grollman A. P. 1991 Insertion of specific bases during DNA synthesis past the oxidation damaged base 8-oxo-dG. Nature349, 431-434.
101. Slupska M. M., Baikolov C., Lloyd R. and Miller J. 1996 Mutator tRNAs are encoded by the Escherichia coli mutator genes mutA and mutC: a novel pathway of mutagenesis. Proc. Natl. Acad. Sci. USA93, 4380-4385.
102. Slupska M. M., King A. G., Lu L. L., Lin R. H., Mao E. F., Lackey C. A. et al. 1998 Examination of the role of DNA polymerase proof reading in the mutator effect of miscoding tRNAs. J. Bacteriol. 180, 5712-5717.
103. Sniegowski P. D., Gerrish P. J., Johnson T. and Shaver A. 2000 The evolution of mutation rates: separating causes from consequences. BioEssays22, 1057-1066.
104. Speyer J. F. 1965 Mutagenic DNA polymerase. Biochem. Biophys. Res. Comm. 21, 6-8.
105. Strauss B. S., Francis R. L. and Pouryadanparast P. 2000 Role of dinB gene product in spontaneous mutation in Eschericha coli with an impaired replicative polymerase. J. Bacteriol. 182, 6742-6750.
106. Studwell-Vaughan P. S. and O'Donnell M. 1993 DNA polymerase accessory protein? is encoded by holE. J. Biol. Chem. 268, 1171-1178.
107. Sundin G. W. and Weigand M. R. 2007 The microbiology of mutability. FEMS Microbiol. Lett. 277, 11-20.
108. Taddie F., Radman M., Maynard-Smith J., Toupance B., Gouyon P. H. and Godelle B. 1997 Role of mutator alleles in adaptive evolution. Nature387, 700-702.
109. Taft-Benz S. A. and Schaaper R. M. 1998 Mutational analysis of the 3′ → 5′ proof reading exonuclease of Escherichia coli DNA polymerase III. Nucleic Acids Res. 26, 4005-4011.
110. Taft-Benz S. A. and Schaaper R. M. 2004 The θ subunit of Escherichia coli DNA polymerase III: a role in stabilizing the e proof reading subunit. J. Bacteriol. 186, 2774-2780.
111. Tajiri T., Maki H. and Sekiguchi M. 1995 Functional cooperation of Mut, MutM and MutY proteins in preventing mutation by spontaneous oxidation of guanine nucleotides in Escherichia coli. Mutat. Res. 336, 257-267.
112. Vandewiele D., Fernandez-de Honestrosa R. A., Timms A. R., Bridges B. A. and Woodgate R. 2002 Sequence analysis and phenotypes of five temperature sensitive mutator alleles of dnaE encoding modified a subunit of Escherichia coli DNA polymerase III holoenzyme. Mutat. Res. 490, 85-95.
113. Wright B. E. 2004 Stressdirected adaptive mutations and evolution. Mol. Microbiol. 52, 643-650.
114. Yamada M., Nunoshiba T., Shimizu M., Gruz P., Kamiya H., Harashima H. et al. 2006 Involvement of Y family DNA polymerases in mutagenesis caused by oxidized nucleotides in Escherichia coli. J. Bacteriol. 188, 4992-4995.
115. Yang W. and Woodgate R. 2007 What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl. Acad. Sci. USA104, 15591-15598.
116. Zhang X., Lu Q., Inouye M. and Marthews C. K. 1996 Effect of T4 phage infection and anaerobiosis upon nucleotide pools and mutagenesis in Ndk defective Escherichia coli strains. J. Bacteriol. 178, 4115-4121.