1887

Abstract

is an opportunistic pathogen known to be resistant to different classes of antibiotics and disinfectants. also displays a certain degree of tolerance to photodynamic therapy (PDT), an alternative antimicrobial approach exploiting a photo-oxidative stress induced by exogenous photosensitizers and visible light. To evaluate whether pigments can contribute to its relative tolerance to PDT, we analysed the response to this treatment of isogenic transposon mutants of PAO1 with altered pigmentation. In general, in the presence of pigments a higher tolerance to PDT-induced photo-oxidative stress was observed. Hyperproduction of pyomelanin makes the cells much more tolerant to stress caused by either radicals or singlet oxygen generated by different photosensitizers upon photoactivation. Phenazines, pyocyanin and phenazine-1-carboxylic acid, produced in different amounts depending on the cultural conditions, are able to counteract both types of PDT-elicited reactive oxygen species. Hyperproduction of pyoverdine, caused by a mutation in a quorum-sensing gene, rendered more tolerant to a photosensitizer that generates mainly singlet oxygen, although in this case the observed tolerance to photo-oxidative stress cannot be exclusively attributed to the presence of the pigment.

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2015-12-01
2019-10-19
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References

  1. Ahuja E. G., Janning P., Mentel M., Graebsch A., Breinbauer R., Hiller W., Costisella B., Thomashow L. S., Mavrodi D. V., Blankenfeldt W.. ( 2008;). PhzA/B catalyzes the formation of the tricycle in phenazine biosynthesis. J Am Chem Soc 130: 17053–17061 [CrossRef] [PubMed].
    [Google Scholar]
  2. Braud A., Hoegy F., Jezequel K., Lebeau T., Schalk I. J.. ( 2009;). New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11: 1079–1091 [CrossRef] [PubMed].
    [Google Scholar]
  3. Brint J. M., Ohman D. E.. ( 1995;). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 177: 7155–7163 [PubMed].
    [Google Scholar]
  4. Caminos D. A., Spesia M. B., Pons P., Durantini E. N.. ( 2008;). Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5,10,15,20-tetra(4-N,N,N-trimethylammoniumphenyl) porphyrin. Photochem Photobiol Sci 7: 1071–1078 [CrossRef] [PubMed].
    [Google Scholar]
  5. Cheluvappa R.. ( 2014;). Standardized chemical synthesis of Pseudomonas aeruginosa pyocyanin. MethodsX 1: 67–73 [CrossRef] [PubMed].
    [Google Scholar]
  6. Diggle S. P., Matthijs S., Wright V. J., Fletcher M. P., Chhabra S. R., Lamont I. L., Kong X., Hider R. C., Cornelis P., other authors. ( 2007;). The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14: 87–96 [CrossRef] [PubMed].
    [Google Scholar]
  7. du Bois R. M.. ( 1985;). The alveolar macrophage. Thorax 40: 321–327 [CrossRef] [PubMed].
    [Google Scholar]
  8. Forbes B. A., Sahm D. F., Weissfeld A. S.. ( 2007;). Bailey and Scott's Diagnostic Microbiology, 12th edn.. St. Louis, MO: C. V. Mosby;.
    [Google Scholar]
  9. Gaonkar T., Nayak P. K., Garg S., Bhosle S.. ( 2012;). Siderophore-producing bacteria from a sand dune ecosystem and the effect of sodium benzoate on siderophore production by a potential isolate. ScientificWorldJournal 2012: 857249 [CrossRef] [PubMed].
    [Google Scholar]
  10. Glaeser J., Klug G.. ( 2005;). Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes. Microbiology 151: 1927–1938 [CrossRef] [PubMed].
    [Google Scholar]
  11. Griffiths M., Sistrom W. R., Cohen-Bazire G., Stanier R. Y.. ( 1955;). Function of carotenoids in photosynthesis. Nature 176: 1211–1214 [CrossRef] [PubMed].
    [Google Scholar]
  12. Hassett D. J., Charniga L., Bean K., Ohman D. E., Cohen M. S.. ( 1992;). Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect Immun 60: 328–336 [PubMed].
    [Google Scholar]
  13. Herrero M., de Lorenzo V., Timmis K. N.. ( 1990;). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557–6567 [PubMed].
    [Google Scholar]
  14. Huang C. T., Shih P. C.. ( 2000;). Effects of quorum sensing signal molecules on the hydrogen peroxide resistance against planktonic Pseudomonas aeruginosa. J Microbiol Immunol Infect 33: 154–158 [PubMed].
    [Google Scholar]
  15. Huang L., Xuan Y., Koide Y., Zhiyentayev T., Tanaka M., Hamblin M. R.. ( 2012;). Type I and Type II mechanisms of antimicrobial photodynamic therapy: an in vitro study on gram-negative and gram-positive bacteria. Lasers Surg Med 44: 490–499 [CrossRef] [PubMed].
    [Google Scholar]
  16. Hunter R. C., Newman D. K.. ( 2010;). A putative ABC transporter, hatABCDE, is among molecular determinants of pyomelanin production in Pseudomonas aeruginosa. J Bacteriol 192: 5962–5971 [CrossRef] [PubMed].
    [Google Scholar]
  17. Jayaseelan S., Ramaswamy D., Dharmaraj S.. ( 2014;). Pyocyanin: production, applications, challenges and new insights. World J Microbiol Biotechnol 30: 1159–1168 [CrossRef] [PubMed].
    [Google Scholar]
  18. Jimenez P. N., Koch G., Thompson J. A., Xavier K. B., Cool R. H., Quax W. J.. ( 2012;). The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76: 46–65 [CrossRef] [PubMed].
    [Google Scholar]
  19. Kahn M., Kolter R., Thomas C., Figurski D., Meyer R., Remaut E., Helinski D. R.. ( 1979;). Plasmid cloning vehicles derived from plasmids ColE1, F, R6K, and RK2. Methods Enzymol 68: 268–280 [CrossRef] [PubMed].
    [Google Scholar]
  20. Kasimova K. R., Sadasivam M., Landi G., Sarna T., Hamblin M. R.. ( 2014;). Potentiation of photoinactivation of Gram-positive and Gram-negative bacteria mediated by six phenothiazinium dyes by addition of azide ion. Photochem Photobiol Sci 13: 1541–1548 [CrossRef] [PubMed].
    [Google Scholar]
  21. Ketelboeter L. M., Potharla V. Y., Bardy S. L.. ( 2014;). NTBC treatment of the pyomelanogenic Pseudomonas aeruginosa clinical isolate PA1111 inhibits pigment production and increases sensitivity to oxidative stress. Curr Microbiol 69: 343–348 [CrossRef] [PubMed].
    [Google Scholar]
  22. King E. O., Ward M. K., Raney D. E.. ( 1954;). Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301–307 [PubMed].
    [Google Scholar]
  23. Kulasekara H. D., Ventre I., Kulasekara B. R., Lazdunski A., Filloux A., Lory S.. ( 2005;). A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55: 368–380 [CrossRef] [PubMed].
    [Google Scholar]
  24. Kurian N. K., Nair H. P., Bath S. G.. ( 2014;). Melanin producing Pseudomonas stutzeri BTCZ10 from marine sediment at 96 m depth (SagarSampada cruise # 305). Int J Curr Biotech 2: 6–11.
    [Google Scholar]
  25. Lau G. W., Hassett D. J., Ran H., Kong F.. ( 2004;). The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10: 599–606 [CrossRef] [PubMed].
    [Google Scholar]
  26. Lee J., Zhang L.. ( 2015;). The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6: 26–41 [CrossRef] [PubMed].
    [Google Scholar]
  27. Mavrodi D. V., Bonsall R. F., Delaney S. M., Soule M. J., Phillips G., Thomashow L. S.. ( 2001;). Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183: 6454–6465 [CrossRef] [PubMed].
    [Google Scholar]
  28. Mavrodi D. V., Parejko J. A., Mavrodi O. V., Kwak Y. S., Weller D. M., Blankenfeldt W., Thomashow L. S.. ( 2013;). Recent insights into the diversity, frequency and ecological roles of phenazines in fluorescent Pseudomonas spp. Environ Microbiol 15: 675–686 [CrossRef] [PubMed].
    [Google Scholar]
  29. Morita Y., Tomida J., Kawamura Y.. ( 2014;). Responses of Pseudomonas aeruginosa to antimicrobials. Front Microbiol 4: 422 [CrossRef] [PubMed].
    [Google Scholar]
  30. Nitzan Y., Kauffman M.. ( 1999;). Endogenous porphyrin production in bacteria by δ-aminolaevulinic acid and subsequent bacterial photoeradication. Lasers Med Sci 14: 269–277 [CrossRef].
    [Google Scholar]
  31. O'Toole G. A., Kolter R.. ( 1998;). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449–461 [CrossRef] [PubMed].
    [Google Scholar]
  32. 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 Bacteriol 182: 4533–4544 [CrossRef] [PubMed].
    [Google Scholar]
  33. Orlandi V. T., Caruso E., Banfi S., Barbieri P.. ( 2012;). Effect of organic matter on the in vitro photoeradication of Pseudomonas aeruginosa by means of a cationic tetraaryl-porphyrin. Photochem Photobiol 88: 557–564 [CrossRef] [PubMed].
    [Google Scholar]
  34. Orlandi V. T., Rybtke M., Caruso E., Banfi S., Tolker-Nielsen T., Barbieri P.. ( 2014;). Antimicrobial and anti-biofilm effect of a novel BODIPY photosensitizer against Pseudomonas aeruginosa PAO1. Biofouling 30: 883–891 [CrossRef] [PubMed].
    [Google Scholar]
  35. Philippova T. O., Galkin B. N., Zinchenko O. Y., Rusakova M. Y., Ivanitsa V. A., Zhilina Z. I., Vodzinskii S. V., Ishkov Y. V.. ( 2003;). The antimicrobial properties of new synthetic porphyrins. J Porphyr Phthalocyanines 07: 755–760 [CrossRef].
    [Google Scholar]
  36. Rada B., Leto T. L.. ( 2013;). Pyocyanin effects on respiratory epithelium: relevance in Pseudomonas aeruginosa airway infections. Trends Microbiol 21: 73–81 [CrossRef] [PubMed].
    [Google Scholar]
  37. Ramel F., Birtic S., Ginies C., Soubigou-Taconnat L., Triantaphylidès C., Havaux M.. ( 2012;). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc Natl Acad Sci U S A 109: 5535–5540 [CrossRef] [PubMed].
    [Google Scholar]
  38. Reszka K. J., Denning G. M., Britigan B. E.. ( 2006;). Photosensitized oxidation and inactivation of pyocyanin, a virulence factor of Pseudomonas aeruginosa. Photochem Photobiol 82: 466–473 [CrossRef] [PubMed].
    [Google Scholar]
  39. Rodríguez-Rojas A., Mena A., Martín S., Borrell N., Oliver A., Blázquez J.. ( 2009;). Inactivation of the hmgA gene of Pseudomonas aeruginosa leads to pyomelanin hyperproduction, stress resistance and increased persistence in chronic lung infection. Microbiology 155: 1050–1057 [CrossRef] [PubMed].
    [Google Scholar]
  40. Stintzi A., Evans K., Meyer J. M., Poole K.. ( 1998;). Quorum-sensing and siderophore biosynthesis in Pseudomonas aeruginosa lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166: 341–345 [CrossRef] [PubMed].
    [Google Scholar]
  41. Stover C. K., Pham X. Q., Erwin A. L., Mizoguchi S. D., Warrener P., Hickey M. J., Brinkman F. S. L., Hufnagle W. O., Kowalik D. J., other authors. ( 2000;). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959–964 [CrossRef] [PubMed].
    [Google Scholar]
  42. Tavares A., Dias S. R., Carvalho C. M., Faustino M. A., Tomé J. P., Neves M. G., Tomé A. C., Cavaleiro J. A., Cunha Â., other authors. ( 2011;). Mechanisms of photodynamic inactivation of a gram-negative recombinant bioluminescent bacterium by cationic porphyrins. Photochem Photobiol Sci 10: 1659–1669 [CrossRef] [PubMed].
    [Google Scholar]
  43. Tegos G. P., Anbe M., Yang C., Demidova T. N., Satti M., Mroz P., Janjua S., Gad F., Hamblin M. R.. ( 2006;). Protease-stable polycationic photosensitizer conjugates between polyethyleneimine and chlorin(e6) for broad-spectrum antimicrobial photoinactivation. Antimicrob Agents Chemother 50: 1402–1410 [CrossRef] [PubMed].
    [Google Scholar]
  44. Vasanthabharathi V., Lakshminarayanan R., Jayalakshmi S.. ( 2011;). Melanin production from marine Streptomyces. Afr J Biotechnol 10: 11224–11234.
    [Google Scholar]
  45. Visca P., Imperi F., Lamont I. L.. ( 2007;). Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15: 22–30 [CrossRef] [PubMed].
    [Google Scholar]
  46. Wainwright M.. ( 1998;). Photodynamic antimicrobial chemotherapy (PACT). J Antimicrob Chemother 42: 13–28 [CrossRef] [PubMed].
    [Google Scholar]
  47. Whiteley M., Lee K. M., Greenberg E. P.. ( 1999;). Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96: 13904–13909 [CrossRef] [PubMed].
    [Google Scholar]
  48. Ziegelhoffer E. C., Donohue T. J.. ( 2009;). Bacterial responses to photo-oxidative stress. Nat Rev Microbiol 7: 856–863 [PubMed].
    [Google Scholar]
  49. Zughaier S. M., Ryley H. C., Jackson S. K.. ( 1999;). A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocyte respiratory burst activity by scavenging superoxide anion. Infect Immun 67: 908–913 [PubMed].
    [Google Scholar]
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