1887

Abstract

Solar UVA radiation is one of the main environmental stress factors for . Exposure to high UVA doses produces lethal effects by the action of the reactive oxygen species (ROS) it generates. has several enzymes, including KatA and KatB catalases, which provide detoxification of ROS. We have previously demonstrated that KatA is essential in defending against high UVA doses. In order to analyse the mechanisms involved in the adaptation of this micro-organism to UVA, we investigated the effect of exposure to low UVA doses on KatA and KatB activities, and the physiological consequences. Exposure to UVA induced total catalase activity; assays with non-denaturing polyacrylamide gels showed that both KatA and KatB activities were increased by radiation. This regulation occurred at the transcriptional level and depended, at least partly, on the increase in HO levels. We demonstrated that exposure to low UVA produced a protective effect against subsequent lethal doses of UVA, sodium hypochlorite and HO. Protection against lethal UVA depends on , whilst protection against sodium hypochlorite depends on , demonstrating that different mechanisms are involved in the defence against these oxidative agents, although both genes can be involved in the global cellular response. Conversely, protection against lethal doses of HO could depend on induction of both genes and/or (an)other defensive factor(s). A better understanding of the adaptive response of to UVA is relevant from an ecological standpoint and for improving disinfection strategies that employ UVA or solar irradiation.

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2016-05-01
2020-01-29
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References

  1. Aebi H.. 1984; Catalase in vitro . In Methods in Enzymology pp121–126 Edited by Parker L.. London: Academic Press;
    [Google Scholar]
  2. Bäumler W., Regensburger J., Knak A., Felgenträger A., Maisch T.. 2012; UVA and endogenous photosensitizers – the detection of singlet oxygen by its luminescence. Photochem Photobiol Sci11:107–117 [CrossRef][PubMed]
    [Google Scholar]
  3. Berney M., Weilenmann H.-U., Egli T.. 2006a; Gene expression of Escherichia coli in continuous culture during adaptation to artificial sunlight. Environ Microbiol8:1635–1647 [CrossRef][PubMed]
    [Google Scholar]
  4. Berney M., Weilenmann H.-U., Ihssen J., Bassin C., Egli T.. 2006b; Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection. Appl Environ Microbiol72:2586–2593 [CrossRef][PubMed]
    [Google Scholar]
  5. Brown S. M., Howell M. L., Vasil M. L., Anderson A. J., Hassett D. J.. 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 Bacteriol177:6536–6544[PubMed]
    [Google Scholar]
  6. Cadenas E., Sies H.. 1984; Low-level chemiluminescence as an indicador of singlet molecular oxygen in biological systems. In Methods in Enzymology pp221–231 Edited by Parker L.. London: Academic Press;
    [Google Scholar]
  7. Cai Y., Strømme M., Welch K.. 2014; Disinfection, kinetics and contribution of reactive oxygen species when eliminating bacteria with TiO2 induced photocatalysis. J Biomater Nanobiotechnol5:200–209 [CrossRef]
    [Google Scholar]
  8. Chamberlain J., Moss S. H.. 1987; Lipid peroxidation and other membrane damage produced in Escherichia coli K1060 by near-UV radiation and deuterium oxide. Photochem Photobiol45:625–630 [CrossRef][PubMed]
    [Google Scholar]
  9. Chang W., Small D. A., Toghrol F., Bentley W. E.. 2005; Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics6:115 [CrossRef][PubMed]
    [Google Scholar]
  10. Costa C. S., Pezzoni M., Fernández R. O., Pizarro R. A.. 2010; Role of the quorum sensing mechanism in the response of Pseudomonas aeruginosa to lethal and sublethal UVA irradiation. Photochem Photobiol86:1334–1342 [CrossRef][PubMed]
    [Google Scholar]
  11. Eisenstark A.. 1970; Sensitivity of Salmonella typhimurium recombinationless (rec) mutants to visible and near-visible light. Mutat Res10:1–6 [CrossRef][PubMed]
    [Google Scholar]
  12. Eisenstark A., Perrot G.. 1987; Catalase has only a minor role in protection against near-ultraviolet radiation damage in bacteria. Mol Gen Genet207:68–72 [CrossRef][PubMed]
    [Google Scholar]
  13. Gamage J., Zhang Z.. 2010; Applications of photocatalytic disinfection. Int J Photoenergy2010:764870 [CrossRef]
    [Google Scholar]
  14. Girard P. M., Francesconi S., Pozzebon M., Graindorge D., Rochette P., Drouin R., Sage E.. 2011; UVA-induced damage to DNA and proteins: direct versus indirect photochemical processes. J Phys Conf Ser261:012002 [CrossRef]
    [Google Scholar]
  15. Hartman P. S.. 1986; In situ hydrogen peroxide production may account for a portion of NUV (300–400 nm) inactivation of stationary phase Escherichia coli . Photochem Photobiol43:87–89 [CrossRef][PubMed]
    [Google Scholar]
  16. Hassett D. J., Woodruff W. A., Wozniak D. J., Vasil M. L., Cohen M. S., Ohman D. E.. 1993; Cloning and characterization of the Pseudomonas aeruginosa sodA and sodB genes encoding manganese- and iron-cofactored superoxide dismutase: demonstration of increased manganese superoxide dismutase activity in alginate-producing bacteria. J Bacteriol175:7658–7665[PubMed]
    [Google Scholar]
  17. Hassett D. J., Alsabbagh E., Parvatiyar K., Howell M. L., Wilmott R. W., Ochsner U. A.. 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 Bacteriol182:4557–4563 [CrossRef][PubMed]
    [Google Scholar]
  18. Heo Y. J., Chung I. Y., Cho W. J., Lee B. Y., Kim J. H., Choi K. H., Lee J. W., Hassett D. J., Cho Y. H.. 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 Bacteriol192:381–390 [CrossRef][PubMed]
    [Google Scholar]
  19. Hoerter J., Eisenstark A., Touati D.. 1989; Mutations by near-ultraviolet radiation in Escherichia coli strains lacking superoxide dismutase. Mutat Res215:161–165 [CrossRef][PubMed]
    [Google Scholar]
  20. Hoerter J. D., Arnold A. A., Kucczynska D. A., Shibuya A., Ward C. S., Sauer M. G., Gizachew A., Hotchkiss T. M., Fleming T. J., other authors. 2005; Effects of sublethal UVA irradiation on activity levels of oxidative defense enzymes and proteins oxidation in Escherichia coli . J Photochem Photobiol B81:171–180[CrossRef]
    [Google Scholar]
  21. Hu M. L., Tappel A. L.. 1992; Potentiation of oxidative damage to proteins by ultraviolet-A and protection by antioxidants. Photochem Photobiol56:357–363 [CrossRef][PubMed]
    [Google Scholar]
  22. Jacobs M. A., Alwood A., Thaipisuttikul I., Spencer D., Haugen E., Ernst S., Will O., Kaul R., Raymond C., other authors. 2003; Comprehensive transposon mutant library of Pseudomonas aeruginosa . Proc Natl Acad Sci U S A100:14339–14344 [CrossRef][PubMed]
    [Google Scholar]
  23. Jiang Y., Dong Y., Luo Q., Li N., Wu G., Gao H.. 2014; Protection from oxidative stress relies mainly on derepression of OxyR-dependent KatB and Dps in Shewanella oneidensis . J Bacteriol196:445–458 [CrossRef][PubMed]
    [Google Scholar]
  24. Khaengraeng R., Reed R. H.. 2005; Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol99:39–50 [CrossRef][PubMed]
    [Google Scholar]
  25. Kidambi S. P., Booth M. G., Kokjohn T. A., Miller R. V.. 1996; recA-dependence of the response of Pseudomonas aeruginosa to UVA and UVB irradiation. Microbiology142:1033–1040 [CrossRef][PubMed]
    [Google Scholar]
  26. Kovach M. E., Elzer P. H., Hill D. S., Robertson G. T., Farris M. A., Roop R. M. II, Peterson K. M.. 1995; Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene166:175–176 [CrossRef][PubMed]
    [Google Scholar]
  27. Kramer G. F., Ames B. N.. 1987; Oxidative mechanisms of toxicity of low-intensity near-UV light in Salmonella typhimurium . J Bacteriol169:2259–2266[PubMed]
    [Google Scholar]
  28. Krych-Madej J., Gebicka L.. 2015; Do pH and flavonoids influence hypochlorous acid-induced catalase inhibition and heme modification?. Int J Biol Macromol80:162–169 [CrossRef][PubMed]
    [Google Scholar]
  29. Larionov A., Krause A., Miller W.. 2005; A standard curve based method for relative real time PCR data processing. BMC Bioinformatics6:62 [CrossRef][PubMed]
    [Google Scholar]
  30. Lee J.-S., Heo Y.-J., Lee J. K., Cho Y.-H.. 2005; KatA, the major catalase, is critical for osmoprotection and virulence in Pseudomonas aeruginosa PA14. Infect Immun73:4399–4403 [CrossRef][PubMed]
    [Google Scholar]
  31. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J.. 1951; Protein measurement with the Folin phenol reagent. J Biol Chem193:265–275[PubMed]
    [Google Scholar]
  32. Ma J.-F., Ochsner U. A., Klotz M. G., Nanayakkara V. K., Howell M. L., Johnson Z., Posey J. E., Vasil M. L., Monaco J. J., Hassett D. J.. 1999; Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa . J Bacteriol181:3730–3742[PubMed]
    [Google Scholar]
  33. Maatouk K., Zaafrane S., Gauthier J. M., Bakhrouf A.. 2004; [Effect of previous culture conditions and the presence of the rpoS gene on the survival of Salmonella typhimurium in sea water exposed to sunlight]. Can J Microbiol50:341–350 (in French) [CrossRef][PubMed]
    [Google Scholar]
  34. Mashino T., Fridovich I.. 1988; Reactions of hypochlorite with catalase. Biochim Biophys Acta956:63–69 [CrossRef][PubMed]
    [Google Scholar]
  35. McDonald L. C., Hackney C. R., Ray B.. 1983; Enhanced recovery of injured Escherichia coli by compounds that degrade hydrogen peroxide or block its formation. Appl Environ Microbiol45:360–365[PubMed]
    [Google Scholar]
  36. McGuigan K. G., Conroy R. M., Mosler H. J., du Preez M., Ubomba-Jaswa E., Fernandez-Ibañez P.. 2012; Solar water disinfection (SODIS): a review from bench-top to roof-top. J Hazard Mater235-236:29–46 [CrossRef][PubMed]
    [Google Scholar]
  37. Miller J. H.. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  38. Miller C. D., Mortensen W. S., Braga G. U. L., Anderson A. J.. 2001; The rpoS gene in Pseudomonas syringae is important in surviving exposure to the near-UV in sunlight. Curr Microbiol43:374–377 [CrossRef][PubMed]
    [Google Scholar]
  39. Mossialos D., Tavankar G. R., Zlosnik J. E., Williams H. D.. 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 Commun341:697–702 [CrossRef][PubMed]
    [Google Scholar]
  40. Ochsner U. A., Vasil M. L., Alsabbagh E., Parvatiyar K., Hassett D. J.. 2000; Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF . J Bacteriol182:4533–4544 [CrossRef][PubMed]
    [Google Scholar]
  41. Pezzoni M., Pizarro R. A., Costa C. S.. 2012; Protective effect of low UVA irradiation against the action of lethal UVA on Pseudomonas aeruginosa: role of the relA gene. J Photochem Photobiol B116:95–104 [CrossRef][PubMed]
    [Google Scholar]
  42. Pezzoni M., Pizarro R. A., Costa C. S.. 2014; Protective role of extracellular catalase (KatA) against UVA radiation in Pseudomonas aeruginosa biofilms. J Photochem Photobiol B131:53–64 [CrossRef][PubMed]
    [Google Scholar]
  43. Pezzoni M., Meichtry M., Pizarro R. A., Costa C. S.. 2015; Role of the Pseudomonas quinolone signal (PQS) in sensitising Pseudomonas aeruginosa to UVA radiation. J Photochem Photobiol B142:129–140 [CrossRef][PubMed]
    [Google Scholar]
  44. Pizarro R. A.. 1995; UVA oxidative damage modified by environmental conditions in Escherichia coli . Int J Radiat Biol68:293–299 [CrossRef][PubMed]
    [Google Scholar]
  45. Qiu X., Sundin G. W., Wu L., Zhou J., Tiedje J. M.. 2005; Comparative analysis of differentially expressed genes in Shewanella oneidensis MR-1 following exposure to UVC, UVB, and UVA radiation. J Bacteriol187:3556–3564 [CrossRef][PubMed]
    [Google Scholar]
  46. Sammartano L. J., Tuveson R. W., Davenport R.. 1986; Control of sensitivity to inactivation by H2O2 and broad-spectrum near-UV radiation by the Escherichia coli katF locus. J Bacteriol168:13–21[PubMed]
    [Google Scholar]
  47. Sassoubre L. M., Ramsey M. M., Gilmore M. S., Boehm A. B.. 2014; Transcriptional response of Enterococcus faecalis to sunlight. J Photochem Photobiol B130:349–356 [CrossRef][PubMed]
    [Google Scholar]
  48. Shennan M. G., Palmer C. M., Schellhorn H. E.. 1996; Role of Fapy glycosylase and UvrABC excinuclease in the repair of UVA (320-400 nm)-mediated DNA damage in Escherichia coli . Photochem Photobiol63:68–73 [CrossRef][PubMed]
    [Google Scholar]
  49. Small D. A., Chang W., Toghrol F., Bentley W. E.. 2007; Toxicogenomic analysis of sodium hypochlorite antimicrobial mechanisms in Pseudomonas aeruginosa . Appl Microbiol Biotechnol74:176–185 [CrossRef][PubMed]
    [Google Scholar]
  50. Soule T., Gao Q., Stout V., Garcia-Pichel F.. 2013; The global response of Nostoc punctiforme ATCC 29133 to UVA stress, assessed in a temporal DNA microarray study. Photochem Photobiol89:415–423 [CrossRef][PubMed]
    [Google Scholar]
  51. Stover C. K., Pham X. Q., Erwin A. L., Mizoguchi S. D., Warrener P., Hickey M. J., Brinkman F. S., Hufnagle W. O., Kowalik D. J., other authors. 2000; Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature406:959–964 [CrossRef][PubMed]
    [Google Scholar]
  52. Su S., Panmanee W., Wilson J. J., Mahtani H. K., Li Q., Vanderwielen B. D., Makris T. M., Rogers M., McDaniel C., other authors. 2014; Catalase (KatA) plays a role in protection against anaerobic nitric oxide in Pseudomonas aeruginosa . PLoS One9:e91813 [CrossRef][PubMed]
    [Google Scholar]
  53. Tilbury R. N., Quickenden T. L.. 1988; Spectral and time dependence studies of the ultraweak bioluminiscence emitted by the bacterium Escherichia coli . Photochem Photobiol47:145–150 [CrossRef]
    [Google Scholar]
  54. Tyrrell R. M.. 1985; A common pathway for protection of bacteria against damage by solar UVA (334 nm, 365 nm) and an oxidising agent (H2O2). Mutat Res145:129–136[PubMed]
    [Google Scholar]
  55. Wayne L. G., Diaz G. A.. 1986; A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels. Anal Biochem157:89–92 [CrossRef][PubMed]
    [Google Scholar]
  56. Webb R. B., Brown M. S.. 1976; Sensitivity of strains of Escherichia coli differing in repair capability to far UV, near UV and visible radiations. Photochem Photobiol24:425–432 [CrossRef][PubMed]
    [Google Scholar]
  57. Wei Q., Minh P. N., Dötsch A., Hildebrand F., Panmanee W., Elfarash A., Schulz S., Plaisance S., Charlier D., other authors. 2012; Global regulation of gene expression by OxyR in an important human opportunistic pathogen. Nucleic Acids Res40:4320–4333 [CrossRef][PubMed]
    [Google Scholar]
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