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Differential expression of the major catalase, KatA in the two wild type Pseudomonas aeruginosa strains, PAO1 and PA14

  • Bi-o Kim
  • In-Young Chung
  • You-Hee ChoEmail author
Article

Abstract

KatA is the major catalase required for hydrogen peroxide (H2O2) resistance and acute virulence in Pseudomonas aeruginosa PA14, whose transcription is governed by its dual promoters (katAp1 and katAp2). Here, we observed that KatA was not required for acute virulence in another wild type P. aeruginosa strain, PAO1, but that PAO1 exhibited higher KatA expression than PA14 did. This was in a good agreement with the observation that PAO1 was more resistant than PA14 to H2O2 as well as to the antibiotic peptide, polymyxin B (PMB), supposed to involve reactive oxygen species (ROS) for its antibacterial activity. The higher KatA expression in PAO1 than in PA14 was attributed to both katAp1 and katAp2 transcripts, as assessed by S1 nuclease mapping. In addition, it was confirmed that the PMB resistance is attributed to both katAp1 and katAp2 in a complementary manner in PA14 and PAO1, by exploiting the promoter mutants for each -10 box (p1m, p2m, and p1p2m). These results provide an evidence that the two widely used P. aeruginosa strains display different virulence mechanisms associated with OxyR and Anr, which need to be further characterized for better understanding of the critical virulence pathways that may differ in various P. aeruginosa strains.

Keywords

Pseudomonas aeruginosa KatA catalase PAO1 PA14 PMB 

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Notes

Acknowledgements

We are grateful to the members of the Cho Lab for their technical assistance and helpful comments. This work was supported by the National Research Foundation of Korea (NRF) Grant (NRF-2017R1A2B3005239).

Supplementary material

References

  1. Arora, S.K., Neely, A.N., Blair, B., Lory, S., and Ramphal, R. 2005. Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect. Immun. 73, 4395–4398.CrossRefGoogle Scholar
  2. Bland, J.M. and Altman, D.G. 2004. The logrank test. BMJ 328, 1073.CrossRefGoogle Scholar
  3. Cady, K.C., Bondy-Denomy, J., Heussler, G.E., Davidson, A.R., and O’Toole, G.A. 2012. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J. Bacteriol. 194, 5728–5738.CrossRefGoogle Scholar
  4. Choi, Y.S., Shin, D.H., Chung, I.Y., Kim, S.H., Heo, Y.J., and Cho, Y.H. 2007. Identification of Pseudomonas aeruginosa genes crucial for hydrogen peroxide resistance. J. Microbiol. Biotechnol. 17, 1344–1352.Google Scholar
  5. Chugani, S., Kim, B.S., Phattarasukol, S., Brittnacher, M.J., Choi, S.H., Harwood, C.S., and Greenberg, E.P. 2012. Strain-dependent diversity in the Pseudomonas aeruginosa quorum-sensing regulon. Proc. Natl. Acad. Sci. USA 109, E2823–E2831.CrossRefGoogle Scholar
  6. Chung, I.Y., Choi, KB., Heo, Y.J., and Cho, Y.H. 2008. Effect of PEL exopolysaccharide on the wspF mutant phenotypes in Pseudomonas aeruginosa PA14. J. Microbiol. Biotechnol. 18, 1227–1234.Google Scholar
  7. Chung, I.Y., Kim, B.O., Jang, H.J., and Cho, Y.H. 2016. Dual promoters of the major catalase (KatA) govern distinct survival strategies of Pseudomonas aeruginosa. Sci. Rep. 6, 31185.CrossRefGoogle Scholar
  8. Clark, S.T., Diaz Caballero, J., Cheang, M., Coburn, B., Wang, P.W., Donaldson, S.L., Zhang, Y., Liu, M., Keshavjee, S., Yau, Y.C., et al. 2015. Phenotypic diversity within a Pseudomonas aeruginosa population infecting an adult with cystic fibrosis. Sci. Rep. 5, 10932.CrossRefGoogle Scholar
  9. Dong, T.G., Dong, S., Catalano, C., Moore, R., Liang, X., and Mekalanos, J.J. 2015. Generation of reactive oxygen species by lethal attacks from competing microbes. Proc. Natl. Acad. Sci. USA 112, 2181–2186.CrossRefGoogle Scholar
  10. Elkins, J.G., Hassett, D.J., Stewart, P.S., Schweizer, H.P., and Mc-Dermott, T.R. 1999. Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65, 4594–4600.Google Scholar
  11. Farinha, M.A. and Kropinski, A.M. 1990. Construction of broad-host-range plasmid vectors for easy visible selection and analysis of promoters. J. Bacteriol. 172, 3496–3499.CrossRefGoogle Scholar
  12. Finnan, S., Morrissey, J.P., O’Gara, F., and Boyd, E.F. 2004. Genome diversity of Pseudomonas aeruginosa isolates from cystic fibrosis patients and the hospital environment. J. Clin. Microbiol. 42, 5783–5792.CrossRefGoogle Scholar
  13. Hassett, D.J., Alsabbagh, E., Parvatiyar, K., Howell, M.L., Wilmott, R.W., and 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. Bacteriol. 182, 4557–4563.CrossRefGoogle Scholar
  14. Hassett, D.J., Ma, J.F., Elkins, J.G., McDermott, T.R., Ochsner, U.A., West, S.E., Huang, C.T., Fredericks, J., Burnett, S., Stewart, P.S., et al. 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.CrossRefGoogle Scholar
  15. He, J., Baldini, R.L., Deziel, E., Saucier, M., Zhang, Q., Liberati, N.T., Lee, D., Urbach, J., Goodman, H.M., and Rahme, L.G. 2004. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc. Natl. Acad. Sci. USA 101, 2530–2535.CrossRefGoogle Scholar
  16. Heo, Y.J., Chung, I.Y., Cho, W.J., Lee, B.Y., Kim, J.H., Choi, K.H., Lee, J.W., Hassett, D.J., and 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. Bacteriol. 192, 381–390.CrossRefGoogle Scholar
  17. Kim, S.H., Lee, B.Y., Lau, G.W., and Cho, Y.H. 2009. IscR modulates catalase A (KatA) activity, peroxide resistance and full virulence of Pseudomonas aeruginosa PA14. J. Microbiol. Biotechnol. 19, 1520–1526.CrossRefGoogle Scholar
  18. Kim, S.H., Park, S.Y., Heo, Y.J., and Cho, Y.H. 2008. Drosophila melanogaster-based screening for multihost virulence factors of Pseudomonas aeruginosa PA14 and identification of a virulence-attenuating factor, HudA. Infect. Immun. 76, 4152–4162.CrossRefGoogle Scholar
  19. Klockgether, J., Cramer, N., Wiehlmann, L., Davenport, C.F., and Tummler, B. 2011. Pseudomonas aeruginosa genomic structure and diversity. Front. Microbiol. 2, 150.CrossRefGoogle Scholar
  20. Lee, J.S., Heo, Y.J., Lee, J.K., and Cho, Y.H. 2005. KatA, the major catalase, is critical for osmoprotection and virulence in Pseudomonas aeruginosa PA14. Infect. Immun. 73, 4399–4403.CrossRefGoogle Scholar
  21. Lee, D.G., Urbach, J.M., Wu, G., Liberati, N.T., Feinbaum, R.L., Miyata, S., Diggins, L.T., He, J., Saucier, M., Deziel, E., et al. 2006. Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol. 7, R90.CrossRefGoogle Scholar
  22. Lutter, E.I., Faria, M.M., Rabin, H.R., and Storey, D.G. 2008. Pseudomonas aeruginosa cystic fibrosis isolates from individual patients demonstrate a range of levels of lethality in two Drosophila melanogaster infection models. Infect. Immun. 76, 1877–1888.CrossRefGoogle Scholar
  23. Sampson, T.R., Liu, X., Schroeder, M.R., Kraft, C.S., Burd, E.M., and Weiss, D.S. 2012. Rapid killing of Acinetobacter baumannii by polymyxins is mediated by a hydroxyl radical death pathway. Antimicrob. Agents Chemother. 56, 5642–5649.CrossRefGoogle Scholar
  24. Seaver, L.C. and Imlay, J.A. 2001. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183, 7173–7181.CrossRefGoogle Scholar
  25. Shin, D.H., Choi, Y.S., and Cho, Y.H. 2008. Unusual properties of catalase A (KatA) of Pseudomonas aeruginosa PA14 are associated with its biofilm peroxide resistance. J. Bacteriol. 190, 2663–2670.CrossRefGoogle Scholar
  26. Suh, S.J., Silo-Suh, L., Woods, D.E., Hassett, D.J., West, S.E., and Ohman, D.E. 1999. Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa. J. Bacteriol. 181, 3890–3897.Google Scholar
  27. Varga, J.J., Barbier, M., Mulet, X., Bielecki, P., Bartell, J.A., Owings, J.P., Martinez-Ramos, I., Hittle, L.E., Davis, M.R.Jr., Damron, F.H., et al. 2015. Genotypic and phenotypic analyses of a Pseudomonas aeruginosa chronic bronchiectasis isolate reveal differences from cystic fibrosis and laboratory strains. BMC Genomics 16, 883.CrossRefGoogle Scholar
  28. Warren, A.E., Boulianne-Larsen, C.M., Chandler, C.B., Chiotti, K., Kroll, E., Miller, S.R., Taddei, F., Sermet-Gaudelus, I., Ferroni, A., McInnerney, K., et al. 2011. Genotypic and phenotypic variation in Pseudomonas aeruginosa reveals signatures of secondary infection and mutator activity in certain cystic fibrosis patients with chronic lung infections. Infect. Immun. 79, 4802–4818.CrossRefGoogle Scholar
  29. Winterbourn, C.C., Hampton, M.B., Livesey, J.H., and Kettle, A.J. 2006. Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing. J. Biol. Chem. 281, 39860–39869.CrossRefGoogle Scholar
  30. Wolfgang, M.C., Kulasekara, B.R., Liang, X., Boyd, D., Wu, K., Yang, Q., Miyada, C.G., and Lory, S. 2003. Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 100, 8484–8489.CrossRefGoogle Scholar
  31. Zegans, M.E., Wozniak, D., Griffin, E., Toutain-Kidd, C.M., Hammond, J.H., Garfoot, A., and Lam, J.S. 2012. Pseudomonas aeruginosa exopolysaccharide Psl promotes resistance to the biofilm inhibitor polysorbate 80. Antimicrob. Agents Chemother. 56, 4112–4122.CrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea 2019

Authors and Affiliations

  1. 1.Department of Pharmacy, College of Pharmacy and Institute of Pharmaceutical SciencesCHA UniversitySeongnamRepublic of Korea

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