Evolution in fast forward: A potential role for mutators in accelerating Staphylococcus aureus pathoadaptation

Journal of Bacteriology

Volumn 195, Issue 3, 2013, Pages 615-628

  Canfield, Gregory S ^a,b   Schwingel, Johanna M ^a   Foley, Matthew H ^a   Vore, Kelly L ^a   Boonanantanasarn, Kanitsak ^a   Gill, Ann L ^a   Sutton, Mark D ^b   Gill, Steven R ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; GUANINE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE;

ADAPTATION; ARTICLE; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CATALYST; CELLULAR STRESS RESPONSE; CHEMOSENSITIVITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE FUNCTION; GENE INACTIVATION; GENE LOSS; GENETIC ANALYSIS; MISMATCH REPAIR; MOLECULAR EVOLUTION; MUTATION RATE; MUTATOR GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; STAPHYLOCOCCUS AUREUS; VIRUS CULTURE;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL TOXINS; BASE SEQUENCE; DNA DAMAGE; DNA MISMATCH REPAIR; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GUANINE; HEMOLYSIN PROTEINS; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; MUTATION; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; STAPHYLOCOCCUS AUREUS; TIME FACTORS; VIRULENCE FACTORS; XANTHOPHYLLS;

EID: 84873048111     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00733-12     Document Type: Article

References (73)

1. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV. 2006. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl. Acad. Sci. U. S. A. 103:8487-8492.
2. Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc. Natl. Acad. Sci. U. S. A. 104:9451-9456.
3. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK. 2007. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298:1763-1771.
4. Novick RP. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429 -1449.
5. Shopsin B, Eaton C, Wasserman GA, Mathema B, Adhikari RP, Agolory S, Altman DR, Holzman RS, Kreiswirth BN, Novick RP. 2010. Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 202:1593-1599.
6. Goerke C, Gressinger M, Endler K, Breitkopf C, Wardecki K, Stern M, Wolz C, Kahl BC. 2007. High phenotypic diversity in infecting but not in colonizing Staphylococcus aureus populations. Environ. Microbiol. 9:3134 -3142.
7. Lattar SM, Tuchscherr LP, Caccuri RL, Centron D, Becker K, Alonso CA, Barberis C, Miranda G, Buzzola FR, von Eiff C, Sordelli DO. 2009. Capsule expression and genotypic differences among Staphylococcus aureus isolates from patients with chronic or acute osteomyelitis. Infect. Immun. 77:1968 -1975.
8. Polosina YY, Cupples CG. 2010. Wot the 'L-Does MutL do? Mutat. Res. 705:228 -238.
9. Prunier AL, Leclercq R. 2005. Role of mutS and mutL genes in hypermutability and recombination in Staphylococcus aureus. J. Bacteriol. 187: 3455-3464.
10. Besier S, Zander J, Kahl BC, Kraiczy P, Brade V, Wichelhaus TA. 2008. The thymidine-dependent small-colony-variant phenotype is associated with hypermutability and antibiotic resistance in clinical Staphylococcus aureus isolates. Antimicrob. Agents Chemother. 52:2183-2189.
11. Michaels ML, Miller JH. 1992. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8- dihydro-8-oxoguanine). J. Bacteriol. 174:6321-6325.
12. Cabrera M, Nghiem Y, Miller JH. 1988. mutM, a second mutator locus in Escherichia coli that generates G.C--T.A transversions. J. Bacteriol. 170:5405-5407.
13. Nghiem Y, Cabrera M, Cupples CG, Miller JH. 1988. The mutY gene: a mutator locus in Escherichia coli that generates G.C--T.A transversions. Proc. Natl. Acad. Sci. U. S. A. 85:2709 -2713.
14. Mandsberg LF, Ciofu O, Kirkby N, Christiansen LE, Poulsen HE, Hoiby N. 2009. Antibiotic resistance in Pseudomonas aeruginosa strains with increased mutation frequency due to inactivation of the DNA oxidative repair system. Antimicrob. Agents Chemother. 53:2483-2491.
15. Prunier AL, Malbruny B, Laurans M, Brouard J, Duhamel JF, Leclercq R. 2003. High rate of macrolide resistance in Staphylococcus aureus strains from patients with cystic fibrosis reveals high proportions of hypermutable strains. J. Infect. Dis. 187:1709 -1716.
16. Yu G. 2010. GenHtr: a tool for comparative assessment of genetic heterogeneity in microbial genomes generated by massive short-read sequencing. BMC Bioinformatics 11:508. doi:10.1186/1471-2105-11-508.
17. Yu G. 2011. Gnom(Cmp): a quantitative approach for comparative analysis of closely related genomes of bacterial pathogens. Genome 54:402-418.
18. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63.
19. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709 -712.
20. Wang RF, Kushner SR. 1991. Construction of versatile low-copynumber vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
21. Gonzalez K, Faustoferri RC, Quivey RG, Jr. 2012. Role of DNA base excision repair in the mutability and virulence of Streptococcus mutans. Mol. Microbiol. 85:361-377.
22. Somerville GA, Beres SB, Fitzgerald JR, DeLeo FR, Cole RL, Hoff JS, Musser JM. 2002. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence. J. Bacteriol. 184:1430 -1437.
23. Hori M, Asanuma T, Inanami O, Kuwabara M, Harashima H, Kamiya H. 2006. Effects of overexpression and antisenseRNAexpression of Orf17, a MutT-type enzyme. Biol. Pharm. Bull. 29:1087-1091.
24. Kamiya H, Iida E, Murata-Kamiya N, Yamamoto Y, Miki T, Harashima H. 2003. Suppression of spontaneous and hydrogen peroxide-induced mutations by a MutT-type nucleotide pool sanitization enzyme, the Escherichia coli Orf135 protein. Genes Cells 8:941-950.
25. Kobayashi M, Ohara-Nemoto Y, Kaneko M, Hayakawa H, Sekiguchi M, Yamamoto K. 1998. Potential of Escherichia coli GTP cyclohydrolase II for hydrolyzing 8-oxo-dGTP, a mutagenic substrate for DNA synthesis. J. Biol. Chem. 273:26394 -26399.
26. Wyrzykowski J, Volkert MR. 2003. The Escherichia coli methyl-directed mismatch repair system repairs base pairs containing oxidative lesions. J. Bacteriol. 185:1701-1704.
27. Elez M, Radman M, Matic I. 2012. Stoichiometry of MutS and MutL at unrepaired mismatches in vivo suggests a mechanism of repair. Nucleic Acids Res. 40:3929 -3938.
28. Nair D, Memmi G, Hernandez D, Bard J, Beaume M, Gill S, Francois P, Cheung AL. 2011. Whole-genome sequencing of Staphylococcus aureus strain RN4220, a key laboratory strain used in virulence research, identifies mutations that affect not only virulence factors but also the fitness of the strain. J. Bacteriol. 193:2332-2335.
29. Pitsikas P, Polosina YY, Cupples CG. 2009. Interaction between the mismatch repair and nucleotide excision repair pathways in the prevention of 5-azacytidine-induced CG-to-GC mutations in Escherichia coli. DNA Repair (Amst) 8:354 -359.
30. Cirz RT, Jones MB, Gingles NA, Minogue TD, Jarrahi B, Peterson SN, Romesberg FE. 2007. Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J. Bacteriol. 189:531-539.
31. Herbert S, Ziebandt AK, Ohlsen K, Schafer T, Hecker M, Albrecht D, Novick R, Gotz F. 2010. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect. Immun. 78:2877-2889.
32. Ryder V. 2010. The mutability of staphylococcal biofilms. Ph.D. thesis. University of Leeds, Leeds, United Kingdom.
33. Aubry-Damon H, Soussy CJ, Courvalin P. 1998. Characterization of mutations in the rpoB gene that confer rifampin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 42:2590 -2594.
34. Yang H, Yung M, Sikavi C, Miller JH. 2011. The role of Bacillus anthracis RecD2 helicase in DNA mismatch repair. DNA Repair (Amst) 10:1121-1130.
35. Zeibell K, Aguila S, Yan Shi V, Chan A, Yang H, Miller JH. 2007. Mutagenesis and repair in Bacillus anthracis: the effect of mutators. J. Bacteriol. 189:2331-2338.
36. López-Olmos K, Hernandez MP, Contreras-Garduno JA, Robleto EA, Setlow P, Yasbin RE, Pedraza-Reyes M. 2012. Roles of endonuclease V, uracil-DNA glycosylase, and mismatch repair in Bacillus subtilis DNA base-deamination-induced mutagenesis. J. Bacteriol. 194:243-252.
37. Gusarov I, Shatalin K, Starodubtseva M, Nudler E. 2009. Endogenous Evolution of Virulence in S. aureus Mutators nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325:1380 -1384.
38. Garibyan L, Huang T, Kim M, Wolff E, Nguyen A, Nguyen T, Diep A, Hu K, Iverson A, Yang H, Miller JH. 2003. Use of the rpoB gene to determine the specificity of base substitution mutations on the Escherichia coli chromosome. DNA Repair (Amst) 2:593-608.
39. Schaaper RM, Dunn RL. 1987. Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors. Proc. Natl. Acad. Sci. U. S. A. 84:6220-6224.
40. Wolff E, Kim M, Hu K, Yang H, Miller JH. 2004. Polymerases leave fingerprints: analysis of the mutational spectrum in Escherichia coli rpoB to assess the role of polymerase IV in spontaneous mutation. J. Bacteriol. 186:2900 -2905.
41. Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC. 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336:315-319.
42. Jain R, Kumar P, Varshney U. 2007. A distinct role of formamidopyrimidine DNA glycosylase (MutM) in down-regulation of accumulation of G, C mutations and protection against oxidative stress in mycobacteria. DNA Repair (Amst) 6:1774 -1785.
43. Tchou J, Kasai H, Shibutani S, Chung MH, Laval J, Grollman AP, Nishimura S. 1991. 8-oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc. Natl. Acad. Sci. U. S. A. 88:4690-4694.
44. Duwat P, de Oliveira R, Ehrlich SD, Boiteux S. 1995. Repair of oxidative DNA damage in gram-positive bacteria: the Lactococcus lactis Fpg protein. Microbiology 141(Pt 2):411-417.
45. Bandaru V, Sunkara S, Wallace SS, Bond JP. 2002. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst) 1:517-529.
46. Matsumoto Y, Zhang QM, Takao M, Yasui A, Yonei S. 2001. Escherichia coli Nth and human hNTH1 DNA glycosylases are involved in removal of 8-oxoguanine from 8-oxoguanine/guanine mispairs in DNA. Nucleic Acids Res. 29:1975-1981.
47. Chang W, Small DA, Toghrol F, Bentley WE. 2006. Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J. Bacteriol. 188:1648 -1659.
48. Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J. Bacteriol. 189:1025-1035.
49. Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ. 2001. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect. Immun. 69:3744-3754.
50. Repine JE, Fox RB, Berger EM. 1981. Hydrogen peroxide kills Staphylococcus aureus by reacting with staphylococcal iron to form hydroxyl radical. J. Biol. Chem. 256:7094 -7096.
51. Watson SP, Clements MO, Foster SJ. 1998. Characterization of the starvation-survival response of Staphylococcus aureus. J. Bacteriol. 180: 1750-1758.
52. Nagorska K, Silhan J, Li Y, Pelicic V, Freemont PS, Baldwin GS, Tang CM. 2012. A network of enzymes involved in repair of oxidative DNA damage in Neisseria meningitidis. Mol. Microbiol. 83:1064 -1079.
53. Richardson AR, Soliven KC, Castor ME, Barnes PD, Libby SJ, Fang FC. 2009. The Base Excision Repair system of Salmonella enterica serovar typhimurium counteracts DNA damage by host nitric oxide. PLoS Pathog. 5:e1000451. doi:10.1371/journal.ppat.1000451.
54. Morikawa K, Ohniwa RL, Kim J, Maruyama A, Ohta T, Takeyasu K. 2006. Bacterial nucleoid dynamics: oxidative stress response in Staphylococcus aureus. Genes Cells 11:409-423.
55. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ. 2007. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797-810.
56. Liu GY, Essex A, Buchanan JT, Datta V, Hoffman HM, Bastian JF, Fierer J, Nizet V. 2005. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med. 202:209 -215.
57. Somerville GA, Proctor RA. 2009. At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci. Microbiol. Mol. Biol. Rev. 73:233-248.
58. Sun F, Liang H, Kong X, Xie S, Cho H, Deng X, Ji Q, Zhang H, Alvarez S, Hicks LM, Bae T, Luo C, Jiang H, He C. 2012. Quorum-sensing agr mediates bacterial oxidation response via an intramolecular disulfide redox switch in the response regulator AgrA. Proc. Natl. Acad. Sci. U. S. A. 109:9095-9100.
59. Daurel C, Prunier AL, Chau F, Garry L, Leclercq R, Fantin B. 2007. Role of hypermutability on bacterial fitness and emergence of resistance in experimental osteomyelitis due to Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 51:344-349.
60. AlcalÁ-Franco B, Montanari S, Cigana C, Bertoni G, Oliver A, Bragonzi A. 2012. Antibiotic pressure compensates the biological cost associated with Pseudomonas aeruginosa hypermutable phenotypes in vitro and in a murine model of chronic airways infection. J. Antimicrob. Chemother. 67:962-969.
61. Gardete S, Kim C, Hartmann BM, Mwangi M, Roux CM, Dunman PM, Chambers HF, Tomasz A. 2012. Genetic pathway in acquisition and loss of vancomycin resistance in a methicillin resistant Staphylococcus aureus (MRSA) strain of clonal type USA300. PLoS Pathog. 8:e1002505. doi:10 .1371/journal.ppat.1002505.
62. Mitchell G, Brouillette E, Seguin DL, Asselin AE, Jacob CL, Malouin F. 2010. A role for sigma factor B in the emergence of Staphylococcus aureus small-colony variants and elevated biofilm production resulting from an exposure to aminoglycosides. Microb. Pathog. 48:18-27.
63. Tuchscherr L, Medina E, Hussain M, Volker W, Heitmann V, Niemann S, Holzinger D, Roth J, Proctor RA, Becker K, Peters G, Loffler B. 2011. Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol. Med. 3:129-141.
64. Schaaff F, Bierbaum G, Baumert N, Bartmann P, Sahl HG. 2003. Mutations are involved in emergence of aminoglycoside-induced small colony variants of Staphylococcus aureus. Int. J. Med. Microbiol. 293: 427-435.
65. Biswas L, Biswas R, Schlag M, Bertram R, Gotz F. 2009. Small-colony variant selection as a survival strategy for Staphylococcus aureus in the presence of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75: 6910-6912.
66. Vesga O, Groeschel MC, Otten MF, Brar DW, Vann JM, Proctor RA. 1996. Staphylococcus aureus small colony variants are induced by the endothelial cell intracellular milieu. J. Infect. Dis. 173:739-742.
67. Kumar P, Henikoff S, Ng PC. 2009. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4:1073-1081.
68. Benson MA, Lilo S, Wasserman GA, Thoendel M, Smith A, Horswill AR, Fraser J, Novick RP, Shopsin B, Torres VJ. 2011. Staphylococcus aureus regulates the expression and production of the staphylococcal superantigen- like secreted proteins in a Rot-dependent manner. Mol. Microbiol. 81:659-675.
69. Ueda T, Kaito C, Omae Y, Sekimizu K. 2011. Sugar-responsive gene expression and the agr system are required for colony spreading in Staphylococcus aureus. Microb. Pathog. 51:178-185.
70. Saravia-Otten P, Muller HP, Arvidson S. 1997. Transcription of Staphylococcus aureus fibronectin binding protein genes is negatively regulated by agr and an agr-independent mechanism. J. Bacteriol. 179:5259-5263.
71. Fowler VG, Jr, Sakoulas G, McIntyre LM, Meka VG, Arbeit RD, Cabell CH, Stryjewski ME, Eliopoulos GM, Reller LB, Corey GR, Jones T, Lucindo N, Yeaman MR, Bayer AS. 2004. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombin-induced platelet microbicidal protein. J. Infect. Dis. 190:1140-1149.
72. Sandoz KM, Mitzimberg SM, Schuster M. 2007. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. U. S. A. 104:15876-15881.
73. Grundmeier M, Tuchscherr L, Bruck M, Viemann D, Roth J, Willscher E, Becker K, Peters G, Loffler B. 2010. Staphylococcal strains vary greatly in their ability to induce an inflammatory response in endothelial cells. J. Infect. Dis. 201:871-880.