Protective role of extracellular catalase (KatA) against UVA radiation in Pseudomonas aeruginosa biofilms

Journal of Photochemistry and Photobiology B: Biology

Volumn 131, Issue , 2014, Pages 53-64

  Pezzoni, Magdalena ^a   Pizarro, Ramón A ^a   Costa, Cristina S ^a  

^a DEPARTAMENTO DE FÍSICA   (Argentina)

Author keywords

Biofilms; Catalase; KatA; Pseudomonas; Ultraviolet A; UVA

Indexed keywords

CATALASE; KATA CATALASE; KATB CATALASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS SUBTILIS; BACTERIOPLANKTON; BACTERIUM CULTURE; BIOFILM; CELL COUNT; CELL MEMBRANE; CELL SURVIVAL; CELL SUSPENSION; CELL VIABILITY; CHEMICAL ANALYSIS; COCULTURE; COLONY FORMING UNIT; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HYPOTHESIS; IRRADIATION; NONHUMAN; OXIDATIVE STRESS; PLASMID; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; ULTRAVIOLET A RADIATION; WILD TYPE; ANIMAL; BOVINE; ENZYMOLOGY; EXTRACELLULAR SPACE; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANKTON; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CATALASE; CATTLE; EXTRACELLULAR SPACE; GENETIC COMPLEMENTATION TEST; PLANKTON; PSEUDOMONAS AERUGINOSA; ULTRAVIOLET RAYS;

EID: 84893453923     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2014.01.005     Document Type: Article

References (71)

1. J.W. Costerton, Z. Lewandowski, D.E. Caldwell, D.R. Korber, and H.M. Lappin-Scott Microbial biofilms Annu. Rev. Microbiol. 49 1995 711 745
2. D.J. Hassett, J.-F. Ma, J.G. Elkins, T.R. McDermott, U.A. Ochsner, S.E.H. West, C.-T. Huang, J. Fredericks, S. Burnett, P.S. Stewart, G. McFeters, L. Passador, and B.H. Iglewski Quorum sensing in Pseudomonas aeruginosa controls expression of casalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide Mol. Microbiol. 34 1999 1082 1093 (Pubitemid 30000324)
3. T.-F. Mah, B. Pitts, B. Pellock, G.C. Walker, P.S. Stewart, and G.A. O'Toole A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance Nature 426 2003 306 310 (Pubitemid 37463151)
4. G.M. Teitzel, and M.R. Parsek Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa Appl. Environ. Microbiol. 69 2003 2313 2320 (Pubitemid 36443652)
5. J. Chamberlain, and S.H. Moss Lipid peroxidation and other membrane damage produced in Escherichia coli K1060 by near-UV radiation and deuterium oxide Photochem. Photobiol. 45 1987 625 630
6. M.L. Hu, and A.L. Tappel Potentiation of oxidative damage to proteins by ultraviolet-A and protection by antioxidants Photochem. Photobiol. 56 1992 357 363
7. O.J. Oppezzo, C.S. Costa, and R.A. Pizarro Effects of ultraviolet A radiation on survival and growth of Gram negative bacteria Trends Photochem. Photobiol. 13 2011 37 50
8. R.O. Fernández, and R.A. Pizarro Ultraviolet-A lethal effect on Pseudomonas aeruginosa Photochem. Photobiol. 64 1996 334 339
9. R.O. Fernández, and R.A. Pizarro Pseudomonas aeruginosa UV-A-induced effect: influence of salts, nutritional stress and pyocyanine J. Photochem. Photobiol. B: Biol. 50 1999 59 65 (Pubitemid 29360968)
10. S.P. Kidambi, M.G. Booth, T.A. Kokjohn, and R.V. Miller RecA-dependence of the response of Pseudomonas aeruginosa to UVA and UVB irradiation Microbiology 142 1996 1033 1040 (Pubitemid 26139378)
11. C.S. Costa, M. Pezzoni, R.O. Fernández, and R.A. Pizarro Role of the quorum sensing mechanism in the response of Pseudomonas aeruginosa to lethal and sublethal UVA irradiation Photochem. Photobiol. 86 2010 1334 1342
12. M. Pezzoni, R.A. Pizarro, and C.S. Costa Protective effect of low UVA irradiation against the action of lethal UVA on Pseudomonas aeruginosa: rol of the relA gene J. Photochem. Photobiol. B: Biol. 116 2012 95 104
13. K.G. McGuigana, R.M. Conroya, H.J. Moslerb, M. du Preezc, E. Ubomba-Jaswac, and P. Fernandez-Ibañez Solar water disinfection (SODIS): a review from bench-top to roof-top J. Hard. Mater. 235-236 2012 29 46
14. J. Gamage, Z. Zhang, Applications of photocatalytic disinfection, Int. J. Photoenergy, 2010, 11 pages. Article ID 764870, http://dx.doi.org/10.1155/2010/ 764870.
15. M.A. Jacobs, A. Alwood, I. Thaipisuttikul, D. Spencer, E. Haugen, S. Ernst, O. Will, R. Kaul, C. Raymond, R. Levy, L. Chun-Rong, D. Guenthner, D. Bovee, M.V. Olson, and C. Manoil Comprehensive transposon mutant library of Pseudomonas aeruginosa Proc. Natl. Acad. Sci. USA 100 2003 14339 14344 (Pubitemid 37499238)
16. K.I. Dantur, and R.A. Pizarro Effect of growth phase on the Escherichia coli response to ultraviolet-A radiation: influence of conditioned media, hydrogen peroxide and acetate J. Photochem. Photobiol. B: Biol. 75 2004 33 39 (Pubitemid 38987008)
17. M. Berney, H.-U. Weilenmann, J. Ihssen, C. Bassin, and T. Egli Specific growth rate determines the sensitivity of Escherichia coli to thermal, UVA, and solar disinfection Appl. Environ. Microb. 72 2006 2586 2593
18. J.-F. Ma, U.A. Ochsner, M.G. Klotz, V.K. Nanayakkara, M.L. Howell, Z. Johnson, J.E. Posey, M.L. Vasil, J.J. Monaco, and D.J. Hassett Bacterioferritin A modulates catalase A (KatA) activity and resistance to hydrogen peroxide in Pseudomonas aeruginosa J. Bacteriol. 181 1999 3730 3742 (Pubitemid 29283801)
19. J.H. Merritt, D.E. Kadouri, and G.A. O'Toole Growing and analyzing static biofilms Curr. Protoc. Microbiol. Unit 1B.1 2005 pp. 1B.1.1-1B.1.17
20. J.D. Hoerter, A.A. Arnold, D.A. Kucczynska, A. Shibuya, C.S. Ward, M.G. Sauer, A. Gizachew, T.M. Hotchkiss, T.J. Fleming, and S. Johnson Effects of sublethal UVA irradiation on activity levels of oxidative defense enzymes and proteins oxidation in Escherichia coli J. Photochem. Photobiol. B:Biol. 81 2005 171 180 (Pubitemid 41722589)
21. A. Polo, M.V. Diamanti, T. Bjarnsholt, N. Høiby, F. Villa, M.P. Pedeferri, and F. Cappitelli Effects of photoactivated titanium dioxide nanopowders and coating on planktonic and biofilm growth of Pseudomonas aeruginosa Photochem. Photobiol. 87 2011 1387 1394
22. K. Smith, and I.S. Hunter Efficacy of common hospital biocides with biofilms of multi-drug resistant clinical isolates J. Med. Microbiol. 57 2008 966 973
23. W.-S. Chang, M. van de Mortel, L. Nielsen, G. Nino de Guzman, X. Li, and L.J. Halverson Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions J. Bacteriol. 189 2007 8290 8299 (Pubitemid 350178941)
24. P. Tielen, F. Roseneau, S. Wilhelm, K.-E. Jaeger, H.-C. Flemming, and J. Wingender Extracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa Microbiology 156 2010 2239 2252
25. C.A. Knutson, and A. Jeanes A new modification of the carbazole analysis: application to heteropolysaccharides Anal. Biochem. 24 1968 470 481
26. S. Ma, U. Selvaraj, D.E. Ohman, R. Quarless, D.J. Hassett, and D.J. Wozniak Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa J. Bacteriol. 180 1998 956 968 (Pubitemid 28084224)
27. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin-Phenol reagents J. Biol. Chem. 193 1951 265 275
28. M. Dubois, K.A. Gilles, J.K. Hamilton, P.A. Rebers, and F. Smith Colorimetric method for determination of sugars and related substances Anal. Chem. 28 1956 350 356
29. H. Aebi, Catalase in Vitro, in: L. Parker (Ed.), Methods in Enzymology, Academic Press, London, vol. 105, 1984, pp. 121-126.
30. L.G. Wayne, and G.A. Diaz A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels Anal. Biochem. 157 1986 89 92
31. S.M. Brown, M.L. Howell, M.L. Vasil, A.J. Anderson, and D.J. Hassett 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 1995 6536 6544
32. J.G. Elkins, D.J. Hassett, P.S. Stewart, H.P. Schweizer, and T.R. McDermott Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide Appl. Environ. Microbiol. 65 1999 4594 4600
33. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual second ed. 1989 Cold Spring Harbor Laboratory, Cold Spring Harbor New York
34. C.K. Stover, X.Q. Pham, A.L. Erwin, S.D. Mizoguchi, P. Warrener, M.J. Hickey, F.S. Brinkman, W.O. Hufnagle, D.J. Kowalik, M. Lagrou, R.L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L.L. Brody, S.N. Coulter, K.R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G.K. Wong, Z. Wu, I.T. Paulsen, J. Reizer, M.H. Saier, R.E. Hancock, S. Lory, and M.V. Olson Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen Nature 406 2000 959 964
35. Y.J. Heo, I.Y. Chung, W.J. Cho, B.Y. Lee, J.H. Kim, K.H. Choi, J.W. Lee, D.J. Hassett, and Y.H. Cho 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 2010 381 390
36. M.E. Kovach, P.H. Elzer, D.S. Hill, G.T. Robertson, M.A. Farris, R.M. Roop II, and K.M. Peterson Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes Gene 166 1995 175 176
37. D.J. Hassett, L. Charniga, K. Bean, D.E. Ohman, and M.S. Cohen Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase Infect. Immun. 60 1992 328 336
38. J.-S. Lee, Y.-J. Heo, J.K. Lee, and Y.-H. Cho KatA, the major catalase, is critical for osmoprotection and virulence in Pseudomonas aeruginosa PA14 Infec. Immun. 73 2005 4399 4403 (Pubitemid 40923188)
39. D. Mossialos, G.R. Tavankar, J.E. Zlosnik, and H.D. Williams 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 2006 697 702 (Pubitemid 43177545)
40. D.J. Hassett, E. Alsabbagh, K. Parvatiyar, M.L. Howell, R.W. Wilmott, and U.A. Ochsner 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 2000 4557 4563 (Pubitemid 30599819)
41. H.N. Kirkman, and G.F. Gaetani Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH Proc. Natl. Acad. Sci. USA 81 1984 4343 4347 (Pubitemid 14052441)
42. S.S. Branda, F. Chu, D.B. Kearns, R. Losick, and R. Kolter A major protein component of the Bacillus subtilis biofilm matrix Mol. Microbiol. 59 2006 1229 1238
43. T. Matsunaga, R. Tomada, T. Nakajima, and H. Wake Photoelectrochemical sterilization of microbial cells by semiconductor powders FEMS Microbiol. Lett. 29 1985 211 214 (Pubitemid 16221826)
44. 2 based thin films FEMS Microbiol. Lett. 211 2002 183 188 (Pubitemid 34655610)
45. S. Malato, P. Fernández-Ibáñez, M.I. Maldonado, J. Blanco, and W. Gernjak Decontamination and disinfection of water by solar photocatalysis: recent overview and trends Catal. Today 147 2009 1 59
46. J.P. Gage, T.M. Roberts, and J.E. Duffy Susceptibility of Pseudomonas aeruginosa biofilm to UV-A illumination over photocatalytic and non-photocatalytic surfaces Biofilms 2 2005 155 163 (Pubitemid 43667916)
47. P.S. Stewart, F. Roe, J. Rayner, J.G. Elkins, Z. Lewandowski, U.A. Ochsner, and D.J. Hassett Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms Appl. Environ. Microbiol. 66 2000 836 838 (Pubitemid 30082784)
48. D.-H. Shin, Y.-S. Choi, and Y.-H. Cho Unusual properties of catalase A (KatA) of Pseudomonas aeruginosa PA14 are associate with its biofilm peroxide resistance J. Bacteriol. 190 2008 2663 2670 (Pubitemid 351508166)
49. J.R. Frederick, J.G. Elkins, N. Bollinger, D.J. Hassett, and T.R. McDermott Factors affecting catalase expression in Pseudomonas aeruginosa biofilms and planktonic cells Appl. Environ. Microbiol. 67 2001 1375 1379 (Pubitemid 33643585)
50. L.J. Sammartano, and R.W. Tuveson The effects of exogenous catalase on broad-spectrum near-UV (300-400 nm) treated Escherichia coli cells Photochem. Photobiol. 40 1984 607 612
51. A. Einserstark, and G. Perrot Catalase has only a minor role in protection against near-ultraviolet radiation damage in bacteria Mol. Gen. Genet. 207 1987 68 72 (Pubitemid 17060372)
52. R.L. Mitchell, and I.C. Anderson Catalase photoinactivation Science 150 1965 74
53. S. Zigman, J. Reddan, J.B. Schultz, and T. McDaniel Structural and functional changes in catalase induced by near-UV radiation Photochem. Photobiol. 63 1996 818 824 (Pubitemid 126467646)
54. M. Aubailly, J. Haigle, A. Giordani, P. Morlière, and R. Santus UV photolysis of catalase revisited: a spectral study of photolytic intermediates J. Photochem. Photobiol. B: Biol. 56 2000 61 67
55. M. Berney, H.-U. Weilenmann, and T. Egli Flow-cytometric study of vital cellular functions in Escherichia coli during solar disinfection (SODIS) Microbiology 152 2006 1719 1729
56. F. Bosshard, M. Berney, M. Scheifele, H.-U. Weilenmann, and T. Egli Solar disinfection (SODIS) and subsequent dark storage of Salmonella typhimurium and Shigella flexneri monitored by flow cytometry Microbiology 155 2009 1310 1317
57. M.O. Elasri, and R.V. Miller Study of the response of a biofilm bacterial community to UV radiation Appl. Environ. Microb. 65 1999 2025 2031
58. L. Yang, Y. Liu, H.Wu.N. Høiby, S. Molin, and Z. Song Current understanding of multi-species biofilms Int. J. Oral. Sci. 3 2011 74 81
59. A. Rajasekar, B. Anandkumar, S. Maruthamuthu, Y.P. Ting, and P.K.S.M. Rahman Characterization of corrosive bacterial consortia isolated from petroleum-product-transporting pipelines Appl. Microbiol. Biotechnol. 85 2010 1175 1188
60. H. Mansouri, S.A. Alavi, M. Yari, A study of Pseudomonas aeruginosa bacteria in microbial corrosion, in: 2nd International Conference on Chemical, Ecology and Environmental Sciences (ICCEES'2012) Singapore, April 28-29, 2012.
61. H. Gibson, J.H. Taylor, K.E. Hall, and J.T. Holah Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial biofilms J. Appl. Microbiol. 87 1999 41 48 (Pubitemid 29325531)
62. J.C. Nickel, J.B. Wright, I. Ruseska, T.J. Marrie, C. Whitfield, and J.W. Costerton Antibiotic resistance of Pseudomonas aeruginosa colonizing a urinary catheter in vitro Eur. J. Clin. Microbiol. 4 1985 213 218 (Pubitemid 15070093)
63. M.D. Willcox, N. Harmis, W. Cowell, and T. Holden Bacterial interactions with contact lenses; effects of lens material, lens wear and microbial physiology Biomaterials 22 2001 3235 3247 (Pubitemid 32923330)
64. J. Lam, R. Chan, K. Lam, and J.W. Costerton Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis Infect. Immun. 28 1980 546 556 (Pubitemid 10102095)
65. D.M. Ramsey, and D.J. Wozniak Understanding the control of Pseudomonas aeruginosa alginate synthesis and the infections in cystic fibrosis Mol. Microbiol. 56 2005 309 322 (prospects for management of chronic) (Pubitemid 40516773)
66. L.R. Mulcahy, V.M. Isabella, and K. Lewis Pseudomonas aeruginosa biofilms in disease Microb. Ecol. 2013 10.1007/s00248-013-0297-x
67. T.-F.C. Mah, and G.A. O'Toole Mechanisms of biofilm resistance to antimicrobial agents Trends Microbiol. 9 2001 34 39
68. H.-C. Flemming, and J. Wingender The biofilm matrix Nat. Rev. Microbiol. 8 2010 623 633
69. M. Hentzer, G.M. Teitzel, G.J. Balzer, A. Heydorn, S. Molin, M. Givskov, and M.R. Parsek Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function J. Bacteriol. 183 2001 5395 5401 (Pubitemid 32802613)
70. J.A. Simpson, S.E. Smith, and R.T. Dean Scavenging by alginate of free radicals released by macrophages Free Radical Biol. Med. 6 1989 347 353 (Pubitemid 19096924)
71. L. Yang, K.B. Barken, M.E. Skindersoe, A.B. Christensen, M. Givskov, and T. Tolker-Nielsen Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa Microbiology 153 2007 1318 1328 (Pubitemid 46779988)