The staphylococcus aureus SrrAB regulatory system modulates hydrogen peroxide resistance factors, which imparts protection to aconitase during Aerobic growth

PLoS ONE

Volumn 12, Issue 1, 2017, Pages

  Mashruwala, Ameya A ^a   Boyd, Jeffrey M ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; FERROUS SULFIDE; HYDROGEN PEROXIDE; OXYGEN; BACTERIAL PROTEIN; PEROXIDE REPRESSOR PROTEINS; REPRESSOR PROTEIN; SRRA PROTEIN, STAPHYOLOCOCCUS AUREUS; SRRB PROTEIN, STAPHYOLOCOCCUS AUREUS;

AHPC GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; CELL RESPIRATION; CONCENTRATION (PARAMETERS); DPS GENE; DRUG RESISTANCE; FERMENTATIVE GROWTH; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; IRON CHELATION; KAT GENE; MICROBIAL GROWTH; NONHUMAN; PEROXIDE REGULON REPRESSOR; PROMOTER REGION; REGULON; SCDA GENE; SRRAB TWO COMPONENT REGULATORY SYSTEM; STAPHYLOCOCCUS AUREUS; ANTIBIOTIC RESISTANCE; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; OXIDATIVE STRESS; TRANSCRIPTION INITIATION;

ACONITATE HYDRATASE; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; HYDROGEN PEROXIDE; MICROBIAL SENSITIVITY TESTS; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 85009963085     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0170283     Document Type: Article

References (94)

1. Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998; 339(8):520-32. Epub 1998/08/26. doi: 10.1056/NEJM199808203390806 PMID: 9709046
2. Imlay JA, Fridovich I. Superoxide production by respiring membranes of Escherichia coli. Free Radic Res Commun. 1991; 12-13 Pt 1:59-66. Epub 1991/01/01.
3. Boveris A, Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J. 1973; 134(3):707-16. Epub 1973/07/01. PubMed Central PMCID: PMC1177867. PMID: 4749271
4. Messner KR, Imlay JA. Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J Biol Chem. 2002; 277(45):42563-71. Epub 2002/08/30. doi: 10.1074/jbc.M204958200 PMID: 12200425
5. Messner KR, Imlay JA. The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfite reductase complex of Escherichia coli. J Biol Chem. 1999; 274(15):10119-28. Epub 1999/04/03. PMID: 10187794
6. Imlay JA. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Advances in Microbial Physiology. 2002; 46:111-53. PMID: 12073652
7. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nature Reviews Microbiology. 2013; 11(7):443-54. Epub 2013/05/29. PubMed Central PMCID: PMC4018742. doi: 10.1038/nrmicro3032 PMID: 23712352
8. Djaman O, Outten FW, Imlay JA. Repair of oxidized iron-sulfur clusters in Escherichia coli. J Biol Chem. 2004; 279(43):44590-9. Epub 2004/08/17. doi: 10.1074/jbc.M406487200 PMID: 15308657
9. Kennedy MC, Kent TA, Emptage M, Merkle H, Beinert H, Munck E. Evidence for the formation of a linear [3Fe-4S] cluster in partially unfolded aconitase. J Biol Chem. 1984; 259(23):14463-71. Epub 1984/ 12/10. PMID: 6094558
10. Imlay JA. Iron-sulphur clusters and the problem with oxygen. Mol Microbiol. 2006; 59(4):1073-82. Epub 2006/01/25. MMI5028 [pii]. doi: 10.1111/j.1365-2958.2006.05028.x PMID: 16430685
11. Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol. 2003; 57:395-418. Epub 2003/10/07. doi: 10.1146/annurev.micro.57.030502.090938 PMID: 14527285
12. Song E, Jaishankar GB, Saleh H, Jithpratuck W, Sahni R, Krishnaswamy G. Chronic granulomatous disease: a review of the infectious and inflammatory complications. Clin Mol Allergy. 2011; 9(1):10. Epub 2011/06/01. 1476-7961-9-10 [pii].PubMed Central PMCID: PMC3128843. doi: 10.1186/1476-7961-9-10 PMID: 21624140
13. Clements MO, Watson SP, Foster SJ. Characterization of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. J Bacteriol. 1999; 181(13):3898-903. Epub 1999/06/29. PubMed Central PMCID: PMC93877. PMID: 10383955
14. Armstrong-Buisseret L, Cole MB, Stewart GS. A homologue to the Escherichia coli alkyl hydroperoxide reductase AhpC is induced by osmotic upshock in Staphylococcus aureus. Microbiology. 1995; 141 (Pt 7):1655-61. Epub 1995/07/01.
15. Clements MO, Foster SJ. Stress resistance in Staphylococcus aureus. Trends Microbiol. 1999; 7 (11):458-62. Epub 1999/11/05. S0966-842X(99)01607-8 [pii]. PMID: 10542426
16. Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, et al. 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. 2007; 189(3):1025-35. Epub 2006/11/23. JB.01524-06 [pii] PubMed Central PMCID: PMC1797328. doi: 10. 1128/JB.01524-06 PMID: 17114262
17. Imlay JA. Cellular defenses against superoxide and hydrogen peroxide. Annual Review of Biochemistry. 2008; 77:755-76. Epub 2008/01/05. PubMed Central PMCID: PMC3057177. doi: 10.1146/annurev. biochem.77.061606.161055 PMID: 18173371
18. Gaupp R, Ledala N, Somerville GA. Staphylococcal response to oxidative stress. Front Cell Infect Microbiol. 2012; 2:33. Epub 2012/08/25. PubMed Central PMCID: PMC3417528. doi: 10.3389/fcimb. 2012.00033 PMID: 22919625
19. Liu GY, Essex A, Buchanan JT, Datta V, Hoffman HM, Bastian JF, et al. Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J Exp Med. 2005; 202(2):209-15. Epub 2005/07/13. jem.20050846 [pii].PubMed Central PMCID: PMC2213009. doi: 10.1084/jem.20050846 PMID: 16009720
20. Imlay JA, Chin SM, Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science. 1988; 240(4852):640-2. Epub 1988/04/29. PMID: 2834821
21. Grant RA, Filman DJ, Finkel SE, Kolter R, Hogle JM. The crystal structure of Dps, a ferritin homolog that binds and protects DNA. Nat Struct Biol. 1998; 5(4):294-303. Epub 1998/04/18. PMID: 9546221
22. Park S, You X, Imlay JA. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc Natl Acad Sci U S A. 2005; 102(26):9317-22. Epub 2005/06/22. 0502051102 [pii]. PubMed Central PMCID: PMC1166606. doi: 10.1073/pnas.0502051102 PMID: 15967999
23. Ilari A, Ceci P, Ferrari D, Rossi GL, Chiancone E. Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. Journal of Biological Chemistry. 2002; 277(40):37619-23. doi: 10. 1074/jbc.M206186200 PMID: 12163499
24. Justino MC, Almeida CC, Teixeira M, Saraiva LM. Escherichia coli di-iron YtfE protein is necessary for the repair of stress-damaged iron-sulfur clusters. J Biol Chem. 2007; 282(14):10352-9. Epub 2007/02/ 10. M610656200 [pii]. doi: 10.1074/jbc.M610656200 PMID: 17289666
25. Overton TW, Justino MC, Li Y, Baptista JM, Melo AM, Cole JA, et al. Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J Bacteriol. 2008; 190(6):2004-13. Epub 2008/01/22. JB.01733-07 [pii]. PubMed Central PMCID: PMC2258886. doi: 10.1128/JB.01733-07 PMID: 18203837
26. Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annual Review of Biochemistry. 2000; 69:183-215. doi: 10.1146/annurev.biochem.69.1.183 PMID: 10966457
27. Gao R, Stock AM. Biological insights from structures of two-component proteins. Annu Rev Microbiol. 2009; 63:133-54. Epub 2009/07/07. PubMed Central PMCID: PMC3645274. doi: 10.1146/annurev. micro.091208.073214 PMID: 19575571
28. Deng DM, Liu MJ, ten Cate JM, Crielaard W. The VicRK system of Streptococcus mutans responds to oxidative stress. J Dent Res. 2007; 86(7):606-10. Epub 2007/06/26. 86/7/606 [pii]. PMID: 17586705
29. Hwang S, Kim M, Ryu S, Jeon B. Regulation of oxidative stress response by CosR, an essential response regulator in Campylobacter jejuni. PLoS One. 2011; 6(7):e22300. Epub 2011/08/04. PubMed Central PMCID: PMC3139631. doi: 10.1371/journal.pone.0022300 PMID: 21811584
30. McCluskey J, Hinds J, Husain S, Witney A, Mitchell TJ. A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae. Mol Microbiol. 2004; 51(6):1661-75. Epub 2004/03/11. 3917 [pii]. PMID: 15009893
31. Pragman AA, Yarwood JM, Tripp TJ, Schlievert PM. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. Journal of bacteriology. 2004; 186 (8):2430-8. Epub 2004/04/03. PubMed Central PMCID: PMC412142. doi: 10.1128/JB.186.8.2430-2438.2004 PMID: 15060046
32. Pragman AA, Ji Y, Schlievert PM. Repression of Staphylococcus aureus SrrAB using inducible antisense srrA alters growth and virulence factor transcript levels. Biochemistry. 2007; 46(1):314-21. Epub 2007/01/03. doi: 10.1021/bi0603266 PMID: 17198402
33. Yarwood JM, McCormick JK, Schlievert PM. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J Bacteriol. 2001; 183 (4):1113-23. Epub 2001/02/07. PubMed Central PMCID: PMC94983. doi: 10.1128/JB.183.4.1113-1123.2001 PMID: 11157922
34. Wilde AD, Snyder DJ, Putnam NE, Valentino MD, Hammer ND, Lonergan ZR, et al. Bacterial Hypoxic Responses Revealed as Critical Determinants of the Host-Pathogen Outcome by TnSeq Analysis of Staphylococcus aureus Invasive Infection. PLoS Pathog. 2015; 11(12):e1005341. Epub 2015/12/20. PubMed Central PMCID: PMC4684308. doi: 10.1371/journal.ppat.1005341 PMID: 26684646
35. Ulrich M, Bastian M, Cramton SE, Ziegler K, Pragman AA, Bragonzi A, et al. The staphylococcal respiratory response regulator SrrAB induces ica gene transcription and polysaccharide intercellular adhesin expression, protecting Staphylococcus aureus from neutrophil killing under anaerobic growth conditions. Mol Microbiol. 2007; 65(5):1276-87. Epub 2007/08/19. doi: 10.1111/j.1365-2958.2007.05863.x PMID: 17697253
36. Kinkel TL, Roux CM, Dunman PM, Fang FC. The Staphylococcus aureus SrrAB two-component system promotes resistance to nitrosative stress and hypoxia. MBio. 2013; 4(6):e00696-13. Epub 2013/ 11/14. mBio.00696-13 [pii]. PubMed Central PMCID: PMC3892780. doi: 10.1128/mBio.00696-13 PMID: 24222487
37. Throup JP, Zappacosta F, Lunsford RD, Annan RS, Carr SA, Lonsdale JT, et al. The srhSR gene pair from Staphylococcus aureus: genomic and proteomic approaches to the identification and characterization of gene function. Biochemistry. 2001; 40(34):10392-401. Epub 2001/08/22. PMID: 11513618
38. Richardson AR, Dunman PM, Fang FC. The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol Microbiol. 2006; 61(4):927-39. Epub 2006/07/25. MMI5290 [pii]. doi: 10.1111/j.1365-2958.2006.05290.x PMID: 16859493
39. Richardson AR, Libby SJ, Fang FC. A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science. 2008; 319(5870):1672-6. Epub 2008/03/22. 319/ 5870/1672 [pii]. doi: 10.1126/science.1155207 PMID: 18356528
40. Boles BR, Thoendel M, Roth AJ, Horswill AR. Identification of genes involved in polysaccharide-independent Staphylococcus aureus biofilm formation. PLoS One. 2010; 5(4):e10146. Epub 2010/04/27. PubMed Central PMCID: PMC2854687. doi: 10.1371/journal.pone.0010146 PMID: 20418950
41. Choby JE, Mike LA, Mashruwala AA, Dutter BF, Dunman PM, Sulikowski GA, et al. A Small-Molecule Inhibitor of Iron-Sulfur Cluster Assembly Uncovers a Link between Virulence Regulation and Metabolism in Staphylococcus aureus. Cell Chem Biol. 23(11):1351-61. Epub 2016/10/25. S2451-9456(16) 30347-6 [pii]. doi: 10.1016/j.chembiol.2016.09.012 PMID: 27773628
42. Mashruwala AA, Bhatt S, Poudel S, Boyd ES, Boyd JM. The DUF59 Containing Protein SufT Is Involved in the Maturation of Iron-Sulfur (FeS) Proteins during Conditions of High FeS Cofactor Demand in Staphylococcus aureus. PLoS genetics. 12(8):e1006233. Epub 2016/08/16. PubMed Central PMCID: PMC4982691. doi: 10.1371/journal.pgen.1006233 PMID: 27517714
43. Fuchs S, Pane-Farre J, Kohler C, Hecker M, Engelmann S. Anaerobic gene expression in Staphylococcus aureus. J Bacteriol. 2007; 189(11):4275-89. doi: 10.1128/JB.00081-07 PMID: 17384184
44. Novick RP. Genetic systems in staphylococci. Methods Enzymol. 1991; 204:587-636. Epub 1991/01/ 01. 0076-6879(91)04029-N [pii]. PMID: 1658572
45. Malone CL, Boles BR, Lauderdale KJ, Thoendel M, Kavanaugh JS, Horswill AR. Fluorescent reporters for Staphylococcus aureus. J Microbiol Methods. 2009; 77(3):251-60. Epub 2009/03/07. S0167-7012 (09)00066-9 [pii]. PubMed Central PMCID: PMC2693297. doi: 10.1016/j.mimet.2009.02.011 PMID: 19264102
46. Mashruwala AA, Roberts CA, Bhatt S, May KL, Carroll RK, Shaw LN, et al. Staphylococcus aureus SufT: an essential iron-sulphur cluster assembly factor in cells experiencing a high-demand for lipoic acid. Molecular microbiology. Epub 2016/10/22.
47. Mashruwala AA, Pang YY, Rosario-Cruz Z, Chahal HK, Benson MA, Mike LA, et al. Nfu facilitates the maturation of iron-sulfur proteins and participates in virulence in Staphylococcus aureus. Mol Microbiol. 2015; 95(3):383-409. Epub 2014/11/13. doi: 10.1111/mmi.12860 PMID: 25388433
48. Kennedy MC, Emptage MH, Dreyer JL, Beinert H. The role of iron in the activation-inactivation of aconitase. Journal of Biological Chemistry. 1983; 258(18):11098-105. PMID: 6309829
49. Beers RF Jr., Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952; 195(1):133-40. Epub 1952/03/01. PMID: 14938361
50. McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969; 244(22):6049-55. Epub 1969/11/25. PMID: 5389100
51. Joska TM, Mashruwala A, Boyd JM, Belden WJ. A universal cloning method based on yeast homologous recombination that is simple, efficient, and versatile. J Microbiol Methods. 2014; 100:46-51. Epub 2014/01/15. S0167-7012(13)00364-3 [pii]. doi: 10.1016/j.mimet.2013.11.013 PMID: 24418681
52. Olson BJ, Markwell J. Assays for determination of protein concentration. Curr Protoc Protein Sci. 2007; Chapter 3:Unit 3 4. Epub 2008/04/23.
53. Dukan S, Touati D. Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J Bacteriol. 1996; 178(21):6145-50. Epub 1996/11/01. PubMed Central PMCID: PMC178483. PMID: 8892812
54. Maalej S, Dammak I, Dukan S. The impairment of superoxide dismutase coordinates the derepression of the PerR regulon in the response of Staphylococcus aureus to HOCl stress. Microbiology-Sgm. 2006; 152:855-61.
55. Mahawar M, Tran V, Sharp JS, Maier RJ. Synergistic roles of Helicobacter pylori methionine sulfoxide reductase and GroEL in repairing oxidant-damaged catalase. J Biol Chem. 286(21):19159-69. Epub 2011/04/05. M111.223677 [pii]. PubMed Central PMCID: PMC3099729. doi: 10.1074/jbc.M111.223677 PMID: 21460217
56. Ballal A, Manna AC. Regulation of superoxide dismutase (sod) genes by SarA in Staphylococcus aureus. J Bacteriol. 2009; 191(10):3301-10. Epub 2009/03/17. JB.01496-08 [pii]. PubMed Central PMCID: PMC2687179. doi: 10.1128/JB.01496-08 PMID: 19286803
57. Horsburgh MJ, Clements MO, Crossley H, Ingham E, Foster SJ. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun. 2001; 69(6):3744-54. Epub 2001/05/12. PubMed Central PMCID: PMC98383. doi: 10.1128/IAI.69.6. 3744-3754.2001 PMID: 11349039
58. Bhattacharya M, Das AK. Inverted repeats in the promoter as an autoregulatory sequence for TcrX in Mycobacterium tuberculosis. Biochemical and Biophysical Research Communications. 2011; 415 (1):17-23. doi: 10.1016/j.bbrc.2011.09.143 PMID: 22001925
59. Wosten MMSM Groisman EA. Molecular characterization of the PmrA regulon. Journal of Biological Chemistry. 1999; 274(38):27185-90. PMID: 10480935
60. Glover RT, Kriakov J, Garforth SJ, Baughn AD, Jacobs WR. The two-component regulatory system senX3-regX3 regulates phosphate-dependent gene expression in Mycobacterium smegmatis. Journal of bacteriology. 2007; 189(15):5495-503. doi: 10.1128/JB.00190-07 PMID: 17526710
61. Eraso JM, Kaplan S. Half-Site DNA Sequence and Spacing Length Contributions to PrrA Binding to PrrA Site 2 of RSP3361 in Rhodobacter sphaeroides 2.4.1. Journal of bacteriology. 2009; 191 (13):4353-64. doi: 10.1128/JB.00244-09 PMID: 19411326
62. de Been M, Bart MJ, Abee T, Siezen RJ, Francke C. The identification of response regulator-specific binding sites reveals new roles of two-component systems in Bacillus cereus and closely related low-GC Gram-positives. Environmental Microbiology. 2008; 10(10):2796-809. doi: 10.1111/j.1462-2920. 2008.01700.x PMID: 18662309
63. Windham IH, Chaudhari SS, Bose JL, Thomas VC, Bayles KW. SrrAB modulates Staphylococcus aureus cell death through regulation of cidABC transcription. J Bacteriol. Epub 2016/01/27. JB.00954-15 [pii].
64. Oogai Y, Kawada-Matsuo M, Komatsuzawa H. Staphylococcus aureus SrrAB Affects Susceptibility to Hydrogen Peroxide and Co-Existence with Streptococcus sanguinis. PloS one. 11(7):e0159768. Epub 2016/07/22. PubMed Central PMCID: PMC4956065. doi: 10.1371/journal.pone.0159768 PMID: 27441894
65. Somerville GA, Said-Salim B, Wickman JM, Raffel SJ, Kreiswirth BN, Musser JM. Correlation of acetate catabolism and growth yield in Staphylococcus aureus: implications for host-pathogen interactions. Infect Immun. 2003; 71(8):4724-32. Epub 2003/07/23. PubMed Central PMCID: PMC166023. doi: 10. 1128/IAI.71.8.4724-4732.2003 PMID: 12874354
66. Ledala N, Zhang B, Seravalli J, Powers R, Somerville GA. Influence of Iron and Aeration on Staphylococcus aureus Growth, Metabolism, and Transcription. J Bacteriol. 2014; 196(12):2178-89. Epub 2014/04/08. JB.01475-14 [pii] 10.1128/JB.01475-14. PubMed Central PMCID: PMC4054190. doi: 10. 1128/JB.01475-14 PMID: 24706736
67. Somerville GA, Proctor RA. Cultivation conditions and the diffusion of oxygen into culture media: the rationale for the flask-to-medium ratio in microbiology. BMC Microbiol. 13:9. Epub 2013/01/18. 1471-2180-13-9 [pii]. PubMed Central PMCID: PMC3551634. doi: 10.1186/1471-2180-13-9 PMID: 23324109
68. McDaniel LE, Bailey EG, Zimmerli A. Effect of Oxygen-Supply Rates on Growth of Escherichia Coli. Ii. Comparison of Results in Shake Flasks and 50-Liter Fermentor. Appl Microbiol. 1965; 13:115-9. Epub 1965/01/01. PubMed Central PMCID: PMC1058203. PMID: 14264839
69. McDaniel LE, Bailey EG, Zimmerli A. Effect of Oxygen Supply Rates on Growth of Escherichia Coli. Appl Microbiol. 1965; 13:109-14. Epub 1965/01/01. PubMed Central PMCID: PMC1058202. PMID: 14264837
70. Benov L, Fridovich I. Growth in iron-enriched medium partially compensates Escherichia coli for the lack of manganese and iron superoxide dismutase. J Biol Chem. 1998; 273(17):10313-6. Epub 1998/ 05/30. PMID: 9553085
71. Benov L, Fridovich I. Why superoxide imposes an aromatic amino acid auxotrophy on Escherichia coli. The transketolase connection. J Biol Chem. 1999; 274(7):4202-6. Epub 1999/02/06. PMID: 9933617
72. Jang S, Imlay JA. Hydrogen peroxide inactivates the Escherichia coli Isc iron-sulphur assembly system, and OxyR induces the Suf system to compensate. Mol Microbiol. 2010; 78(6):1448-67. Epub 2010/12/ 15. PubMed Central PMCID: PMC3051806. doi: 10.1111/j.1365-2958.2010.07418.x PMID: 21143317
73. Yankovskaya V, Horsefield R, Tornroth S, Luna-Chavez C, Miyoshi H, Leger C, et al. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science. 2003; 299(5607):700-4. doi: 10.1126/science.1079605 PMID: 12560550
74. Sun F, Liang H, Kong X, Xie S, Cho H, Deng X, et al. 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. 2012; 109(23):9095-100. Epub 2012/05/16. 1200603109 [pii]. PubMed Central PMCID: PMC3384213. doi: 10.1073/pnas.1200603109 PMID: 22586129
75. Nair D, Memmi G, Hernandez D, Bard J, Beaume M, Gill S, et al. 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(9):2332-5. Epub 2011/03/08. JB.00027-11 [pii]. PubMed Central PMCID: PMC3133102. doi: 10.1128/JB.00027-11 PMID: 21378186
76. Memmi G, Nair DR, Cheung A. Role of ArlRS in autolysis in methicillin-sensitive and methicillin-resistant Staphylococcus aureus strains. J Bacteriol. 2012; 194(4):759-67. Epub 2011/12/06. JB.06261-11 [pii]. PubMed Central PMCID: PMC3272946. doi: 10.1128/JB.06261-11 PMID: 22139508
77. Herbert S, Ziebandt AK, Ohlsen K, Schafer T, Hecker M, Albrecht D, et al. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun. 2010; 78(6):2877-89. Epub 2010/03/10. IAI.00088-10 [pii]. PubMed Central PMCID: PMC2876537. doi: 10. 1128/IAI.00088-10 PMID: 20212089
78. Durand S, Braun F, Lioliou E, Romilly C, Helfer AC, Kuhn L, et al. A nitric oxide regulated small RNA controls expression of genes involved in redox homeostasis in Bacillus subtilis. PLoS Genet. 11(2): e1004957. Epub 2015/02/03. doi: 10.1371/journal.pgen.1004957 PMID: 25643072
79. Seaver LC, Imlay JA. Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol. 2001; 183(24):7182-9. Epub 2001/11/22. PubMed Central PMCID: PMC95567. doi: 10.1128/JB.183.24.7182-7189.2001 PMID: 11717277
80. Jang S, Imlay JA. Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging ironsulfur enzymes. J Biol Chem. 2007; 282(2):929-37. Epub 2006/11/15. M607646200 [pii]. doi: 10.1074/ jbc.M607646200 PMID: 17102132
81. Flint DH, Tuminello JF, Emptage MH. The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J Biol Chem. 1993; 268(30):22369-76. Epub 1993/10/25. PMID: 8226748
82. Georgellis D, Kwon O, Lin ECC. Quinones as the redox signal for the Arc two-component system of bacteria. Science. 2001; 292(5525):2314-6. doi: 10.1126/science.1059361 PMID: 11423658
83. Wong SM, Alugupalli KR, Ram S, Akerley BJ. The ArcA regulon and oxidative stress resistance in Haemophilus influenzae. Mol Microbiol. 2007; 64(5):1375-90. Epub 2007/06/05. MMI5747 [pii]. PubMed Central PMCID: PMC1974803. doi: 10.1111/j.1365-2958.2007.05747.x PMID: 17542927
84. Loui C, Chang AC, Lu S. Role of the ArcAB two-component system in the resistance of Escherichia coli to reactive oxygen stress. BMC Microbiol. 2009; 9:183. Epub 2009/09/01. 1471-2180-9-183 [pii]. PubMed Central PMCID: PMC2748088. doi: 10.1186/1471-2180-9-183 PMID: 19715602
85. Lu S, Killoran PB, Fang FC, Riley LW. The global regulator ArcA controls resistance to reactive nitrogen and oxygen intermediates in Salmonella enterica serovar Enteritidis. Infect Immun. 2002; 70(2):451-61. Epub 2002/01/18. PubMed Central PMCID: PMC127680. doi: 10.1128/IAI.70.2.451-461.2002 PMID: 11796570
86. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, et al. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature. 1983; 305 (5936):709-12. Epub 1983/10/20. PMID: 6226876
87. Pang YY, Schwartz J, Bloomberg S, Boyd JM, Horswill AR, Nauseef WM. Methionine sulfoxide reductases protect against oxidative stress in Staphylococcus aureus encountering exogenous oxidants and human neutrophils. J Innate Immun. 2014; 6(3):353-64. Epub 2013/11/20. 000355915 [pii]. PubMed Central PMCID: PMC3972283. doi: 10.1159/000355915 PMID: 24247266
88. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, et al. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. MBio. 2013; 4(1): e00537-12. Epub 2013/02/14. mBio.00537-12 [pii]. PubMed Central PMCID: PMC3573662. doi: 10. 1128/mBio.00537-12 PMID: 23404398
89. Duthie ES, Lorenz LL. Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol. 1952; 6(1-2):95-107. Epub 1952/02/01. doi: 10.1099/00221287-6-1-2-95 PMID: 14927856
90. Horsburgh MJ, Ingham E, Foster SJ. In Staphylococcus aureus, fur is an interactive regulator with PerR, contributes to virulence, and Is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J Bacteriol. 2001; 183(2):468-75. Epub 2001/01/03. PubMed Central PMCID: PMC94901. doi: 10.1128/JB.183.2.468-475.2001 PMID: 11133939
91. Sadykov MR, Mattes TA, Luong TT, Zhu Y, Day SR, Sifri CD, et al. Tricarboxylic acid cycle-dependent synthesis of Staphylococcus aureus Type 5 and 8 capsular polysaccharides. J Bacteriol. 2010; 192 (5):1459-62. Epub 2010/01/12. PubMed Central PMCID: PMC2820852. doi: 10.1128/JB.01377-09 PMID: 20061474
92. Bose JL, Fey PD, Bayles KW. Genetic tools to enhance the study of gene function and regulation in Staphylococcus aureus. Appl Environ Microbiol. 2013; 79(7):2218-24. Epub 2013/01/29. AEM.00136-13 [pii]. PubMed Central PMCID: PMC3623228. doi: 10.1128/AEM.00136-13 PMID: 23354696
93. Forsyth RA, Haselbeck RJ, Ohlsen KL, Yamamoto RT, Xu H, Trawick JD, et al. A genome-wide strategy for the identification of essential genes in Staphylococcus aureus. Mol Microbiol. 2002; 43(6):1387-400. Epub 2002/04/16. 2832 [pii]. PMID: 11952893
94. Mashruwala AA, Boyd JM. De Novo Assembly of Plasmids Using Yeast Recombinational Cloning. Methods Mol Biol. 1373:33-41. Epub 2015/07/22. doi: 10.1007/7651-2015-275 PMID: 26194707