The stringent response controls catalases in Pseudomonas aeruginosa and is required for hydrogen peroxide and antibiotic tolerance

Journal of Bacteriology

Volumn 195, Issue 9, 2013, Pages 2011-2020

  Khakimova, Malika ^a   Ahlgren, Heather G ^a   Harrison, J J ^b,d   English, Ann M ^c   Nguyen, Dao ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Gina Cody School of Engineering and Computer Science   (Canada)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIUM MUTANT; BIOFILM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; GENE OVEREXPRESSION; KATA GENE; KATB GENE; MICROBIOLOGICAL PARAMETERS; MOLECULAR MECHANICS; NONHUMAN; PLANKTON; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; STARVATION; STRINGENT RESPONSE; UPREGULATION; WILD TYPE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CATALASE; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; PSEUDOMONAS AERUGINOSA; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

PSEUDOMONAS AERUGINOSA;

EID: 84876181159     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02061-12     Document Type: Article

References (78)

1. Demple B. 1991. Regulation of bacterial oxidative stress genes. Annu. Rev. Genet. 25:315-337.
2. Imlay JA. 2008. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77:755-776.
3. 2 challenge in Escherichia coli. J. Bacteriol. 170:3910 -3914.
4. Giard J-C, Hartke A, Flahaut S, Benachour A, Boutibonnes P, Auffray Y. 1996. Starvation-induced multiresistance in Enterococcus faecalis JH2-2. Curr. Microbiol. 32:264 -271.
5. Seymour RL, Mishra PV, Khan MA, Spector MP. 1996. Essential roles of core starvation-stress response loci in carbon-starvation-inducible crossresistance and hydrogen peroxide-inducible adaptive resistance to oxidative challenge in Salmonella typhimurium. Mol. Microbiol. 20:497-505.
6. 2 challenge in Vibrio parahaemolyticus. Microbiol. Immunol. 39:213-215.
7. Hassett DJ, Elkins JG, Ma JF, McDermott TR. 1999. Pseudomonas aeruginosa biofilm sensitivity to biocides: use of hydrogen peroxide as model antimicrobial agent for examining resistance mechanisms. Methods Enzymol. 310:599-608.
8. Elkins JG, Hassett DJ, Stewart PS, Schweizer HP, McDermott TR. 1999. Protective role of catalase in Pseudomonas Aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65:4594-4600.
9. Lange R, Hengge-Aronis R. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5:49 -59.
10. Wu J, Xie J. 2009. Magic spot: (p) ppGpp. J. Cell. Physiol. 220:297-302.
11. Cashel M, Gentry DR, Hernandez VJ, Vinella D. 1996. The stringent response, p 1458-1496. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed, vol 1. ASM Press, Washington, DC.
12. Nyström T. 2004. Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol. Microbiol. 54:855- 862.
13. Braeken K, Moris M, Daniels R, Vanderleyden J, Michiels J. 2006. New horizons for (p) ppGpp in bacterial and plant physiology. Trends Microbiol. 14:45-54.
14. Yan X, Zhao C, Budin-Verneuil A, Hartke A, Rincé A, Gilmore MS, Auffray Y, Pichereau V. 2009. The (p)ppGpp synthetase RelA contributes to stress adaptation and virulence in Enterococcus faecalis V583. Microbiology 155:3226 -3237.
15. VanBogelen RA, Kelley PM, Neidhardt FC. 1987. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J. Bacteriol. 169:26 -32.
16. Zamocky M, Furtmuller PG, Obinger C. 2008. Evolution of catalases from bacteria to humans. Antioxid. Redox Signal. 10:1527-1548.
17. Lee J-S, Heo Y-J, Lee JK, Cho Y-H. 2005. KatA, the major catalase, is critical for osmoprotection and virulence in Pseudomonas aeruginosa PA14. Infect. Immun. 73:4399-4403.
18. Kim SH, Lee BY, Lau GW, Cho YH. 2009. IscR modulates catalase A (KatA) activity, peroxide resistance and full virulence of Pseudomonas aeruginosa PA14. J. Microbiol. Biotechnol. 19:1520 -1526.
19. Brown SM, Howell ML, Vasil ML, Anderson AJ, Hassett DJ. 1995. Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J. Bacteriol. 177:6536-6544.
20. Mossialos D, Tavankar GR, Zlosnik JEA, Williams HD. 2006. Defects in a quinol oxidase lead to loss of KatC catalase activity in Pseudomonas aeruginosa: KatC activity is temperature dependent and it requires an intact disulphide bond formation system. Biochem. Biophys. Res. Commun. 341:697-702.
21. Wei Q, Minh PN, Dötsch A, Hildebrand F, Panmanee W, Elfarash A, Schulz S, Plaisance S, Charlier D, Hassett D, Häussler S, Cornelis P. 2012. Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res. 40:4320-4333.
22. Heo Y-J, Chung I-Y, Cho W-J, Lee B-Y, Kim J-H, Choi K-H, Lee JW, Hassett DJ, Cho YH. 2010. The major catalase gene (katA) of Pseudomonas aeruginosa PA14 is under both positive and negative control of the global transactivator OxyR in response to hydrogen peroxide. J. Bacteriol. 192:381-390.
23. Vinckx T, Matthijs S, Cornelis P. 2008. Loss of the oxidative stress regulator OxyR in Pseudomonas aeruginosa PAO1 impairs growth under iron limited conditions. FEMS Microbiol. Lett. 288:258 -265.
24. Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K, Hassett DJ. 2000. Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, andahpC-ahpF. J. Bacteriol. 182:4533- 4544.
25. Panmanee W, Hassett DJ. 2009. Differential roles of OxyR-controlled antioxidant enzymes alkyl hydroperoxide reductase (AhpCF) and catalase (KatB) in the protection of Pseudomonas aeruginosa against hydrogen peroxide in biofilm vs. planktonic culture. FEMS Microbiol. Lett. 295: 238-244.
26. Hassett DJ, Ma JÄ Elkins JG, McDermott TR, Ochsner UA, West SE, Huang CT, Fredericks J, Burnett S, Stewart PS, McFeters G, Passador L, Iglewski BH. 1999. Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol. Microbiol. 34:1082-1093.
27. Bollinger N, Hassett DJ, Iglewski BH, Costerton JW, McDermott TR. 2001. Gene expression in Pseudomonas aeruginosa: evidence of iron override effects on quorum sensing and biofilm-specific gene regulation. J. Bacteriol. 183:1990 -1996.
28. Suh S-J, Silo-Suh L, Woods DE, Hassett DJ, West SEH, Ohman DE. 1999. Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa. J. Bacteriol. 181:3890- 3897.
29. Cochran WL, Suh SJ, McFeters GA, Stewart PS. 2000. Role of RpoS and AlgT in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide and monochloramine. J. Appl. Microbiol. 88:546 -553.
30. Jørgensen F, Bally M, Chapon-Herve V, Michel G, Lazdunski A, Williams P, Stewart GS. 1999. RpoS-dependent stress tolerance in Pseudomonas aeruginosa. Microbiology 145(Pt 4):835- 844.
31. Hassett DJ, Sokol PA, Howell ML, Ma JF, Schweizer HT, Ochsner U, Vasil ML. 1996. Ferric uptake regulator (Fur) mutants of Pseudomonas aeruginosa demonstrate defective siderophore-mediated iron uptake, altered aerobic growth, and decreased superoxide dismutase and catalase activities. J. Bacteriol. 178:3996-4003.
32. Ma J-F, Ochsner UA, Klotz MG, Nanayakkara VK, Howell ML, Johnson Z, Posey JE, Vasil ML, Monaco JJ, Hassett DJ. 1999. Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa. J. Bacteriol. 181:3730 -3742.
33. Nguyen D, Joshi-Datar A, Lepine F, Bauerle E, Olakanmi O, Beer K, McKay G, Siehnel R, Schafhauser J, Wang Y, Britigan BE, Singh PK. 2011. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334:982-986.
34. Dwyer DJ, Kohanski MA, Collins JJ. 2009. Role of reactive oxygen species in antibiotic action and resistance. Curr. Opin. Microbiol. 12:482- 489.
35. 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.
36. Yeom J, Imlay JA, Park W. 2010. Iron homeostasis affects antibioticmediated cell death in Pseudomonas species. J. Biol. Chem. 285:22689- 22695.
37. Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ. 2008. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135:679-690.
38. 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.
39. Tosa T, Pizer LI. 1971. Biochemical bases for the antimetabolite action of L-serine hydroxamate. J. Bacteriol. 106:972-982.
40. Walters MC, III, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. 2003. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob. Agents Chemother. 47:317-323.
41. Held K, Ramage E, Jacobs M, Gallagher L, Manoil C. 2012. Sequenceverified two-allele transposon mutant library for Pseudomonas aeruginosa PAO1. J. Bacteriol. 194:6387- 6389.
42. Choi KH, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
43. Kayama S, Murakami K, Ono T, Ushimaru M, Yamamoto A, Hirota K, Miyake Y. 2009. The role of rpoS gene and quorum sensing system in ofloxacin tolerance in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 298:184 -192.
44. van Delden C, Comte R, Bally AM. 2001. Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. Bacteriol. J. 183:5376 -5384.
45. Siehnel R, Traxler B, An DD, Parsek MR, Schaefer AL, Singh PK. 2010. A unique regulator controls the activation threshold of quorum-regulated genes in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 107: 7916-7921.
46. Choi KH, Schweizer HP. 2006. mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat. Protoc. 1:153-161.
47. Becher Anna SH. 2000. Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 29:948 -952.
48. Hoang TT, Kutchma AJ, Becher A, Schweizer HP. 2000. Integrationproficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid. 43: 59-72.
49. Beers RF, Jr, Sizer IW. 1952. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 195: 133-140.
50. Zhang X, Bremer H. 1995. Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J. Biol. Chem. 270:11181-11189.
51. Mackey BM, Derrick CM. 1986. Peroxide sensitivity of cold-shocked Salmonella typhimurium and Escherichia coli and its relationship to minimal medium recovery. J. Appl. Bacteriol. 60:501-511.
52. Hassan HM, Fridovich I. 1978. Regulation of the synthesis of catalase and peroxidase in Escherichia coli. J. Biol. Chem. 253:6445- 6450.
53. Karlsson M, Kurz T, Brunk UT, Nilsson SE, Frennesson CI. 2010. What does the commonly used DCF test for oxidative stress really show? Biochem. J. 428:183-190.
54. Setsukinai K, Urano Y, Kakinuma K, Majima HJ, Nagano T. 2003. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278:3170-3175.
55. Dalebroux ZD, Swanson MS. 2012. ppGpp: magic beyond RNA polymerase. Nat. Rev. Microbiol. 10:203-212.
56. DiDonato LN, Sullivan SA, Methe BA, Nevin KP, England R, Lovley DR. 2006. Role of RelGsu in stress response and Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 188:8469-8478.
57. Vogt SL, Green C, Stevens KM, Day B, Erickson DL, Woods DE, Storey DG. 2011. The stringent response is essential for Pseudomonas aeruginosa virulence in the rat lung agar bead and Drosophila melanogaster feeding models of infection. Infect. Immun. 79:4094-4104.
58. Seaton K, Ahn Sagstetter S-JAM, Burne RA. 2011. A transcriptional regulator and ABC transporters link stress tolerance, (p)ppGpp, and genetic competence in Streptococcus mutans. J. Bacteriol. 193:862- 874.
59. Vercruysse M, Fauvart M, Jans A, Beullens S, Braeken K, Cloots L, Engelen K, Marchal K, Michiels J. 2011. Stress response regulators identified through genome-wide transcriptome analysis of the (p) ppGppdependent response in Rhizobium etli. Genome Biol. 12:R17. doi:10.1186 /gb-2011-12-2-r17.
60. Erickson DL, Lines JL, Pesci EC, Venturi V, Storey DG. 2004. Pseu- Stringent Response Control of P. aeruginosa Catalases domonas aeruginosa relA contributes to virulence in Drosophila melanogaster. Infect. Immun. 72:5638 -5645.
61. Kvint K, Farewell A, Nystrom T. 2000. RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of sigma (s). J. Biol. Chem. 275:14795-14798.
62. Lange R, Fischer D, Hengge-Aronis R. 1995. Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J. Bacteriol. 177:4676-4680.
63. Bougdour A, Gottesman S. 2007. ppGpp regulation of RpoS degradation via anti-adaptor protein IraP. Proc. Natl. Acad. Sci. U. S. A. 104:12896- 12901.
64. Schuster M, Hawkins AC, Harwood CS, Greenberg EP. 2004. The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol. Microbiol. 51:973-985.
65. Stewart PS, Roe F, Rayner J, Elkins JG, Lewandowski Z, Ochsner UA, Hassett DJ. 2000. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 66:836- 838.
66. Lee C, Lee SM, Mukhopadhyay P, Kim SJ, Lee SC, Ahn WS, Yu MH, Storz G, Ryu SE. 2004. Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat. Struct. Mol. Biol. 11:1179 -1185.
67. Chelikani P, Fita I, Loewen PC. 2004. Diversity of structures and properties among catalases. Cell. Mol. Life Sci. 61:192-208.
68. Frederick JR, Elkins JG, Bollinger N, Hassett DJ, McDermott TR. 2001. Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells. Appl. Environ. Microbiol. 67:1375-1379.
69. Goswami M, Mangoli SH, Jawali N. 2006. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother. 50:949 -954.
70. Hassett DJ, Alsabbagh E, Parvatiyar K, Howell ML, Wilmott RW, Ochsner UA. 2000. A protease-resistant catalase, KatA, released upon cell lysis during stationary phase is essential for aerobic survival of a Pseudomonas aeruginosa oxyR mutant at low cell densities. J. Bacteriol. 182: 4557-4563.
71. Bayir A, Sirkecioglu AN, Bayir M, Haliloglu HI, Kocaman EM, Aras NM. 2011. Metabolic responses to prolonged starvation, food restriction, and refeeding in the brown trout, Salmo trutta: oxidative stress and antioxidant defenses. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 159: 191-196.
72. Morales AE, Perez-Jimenez A, Hidalgo MC, Abellan E, Cardenete G. 2004. Oxidative stress and antioxidant defenses after prolonged starvation in Dentex dentex liver. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 139:153-161.
73. Petti AA, Crutchfield CA, Rabinowitz JD, Botstein D. 2011. Survival of starving yeast is correlated with oxidative stress response and nonrespiratory mitochondrial function. Proc. Natl. Acad. Sci. U. S. A. 108:E1089- E1098.
74. Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz KJ. 2004. The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol. Plant. 120:63-73.
75. Guo M, Block A, Bryan CD, Becker DF, Alfano JR. 2012. Pseudomonas syringae catalases are collectively required for plant pathogenesis. J. Bacteriol. 194:5054 -5064.
76. Hébrard M, Viala JP, Meresse S, Barras F, Aussel L. 2009. Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J. Bacteriol. 191:4605- 4614.
77. Cosgrove K, Coutts G, Jonsson Tarkowski I-MA, 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.
78. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, II, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.