Pseudomonas aeruginosa manipulates redox and iron homeostasis of its microbiota partner Aspergillus fumigatus via phenazines

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Briard, Benoit ^a,b   Bomme, Perrine ^a   Lechner, Beatrix E ^c   Mislin, Gaëtan L A ^d   Lair, Virginie ^e   Prévost, Marie Christine ^a   Latgé, Jean Paul ^a   Haas, Hubertus ^c   Beauvais, Anne ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^d Institut de Recherche de l'Ecole de Biotechnologie de Strasbourg   (France)

^e PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; PHENAZINE DERIVATIVE; REACTIVE NITROGEN SPECIES; SUPEROXIDE;

ASPERGILLUS FUMIGATUS; METABOLISM; MICROFLORA; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA;

ASPERGILLUS FUMIGATUS; IRON; MICROBIOTA; OXIDATION-REDUCTION; PHENAZINES; PSEUDOMONAS AERUGINOSA; REACTIVE NITROGEN SPECIES; SUPEROXIDES;

EID: 84942140357     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08220     Document Type: Article

References (48)

1. Price-Whelan, A., Dietrich, L. E. P., Newman, D. K. Rethinking 'secondary' metabolism: physiological roles for phenazine antibiotics. Nat. Chem. Biol. 2, 71-78 (2006).
2. Gibson, J., Sood, A., Hogan, D. A. Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl. Environ. Microbiol. 75, 504-513 (2009).
3. Lau, G. W., Hassett, D. J., Ran, H., Kong, F. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol. Med. 10, 599-606 (2004).
4. Wilson, R. et al.Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect. Immun. 56, 2515-2517 (1988).
5. Wang, Y., Kern, S. E., Newman, D. K. Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J. Bacteriol. 192, 365-369 (2010).
6. Cezairliyan, B. et al. Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog. 9, e1003101 (2013).
7. Muller, M. Pyocyanin induces oxidative stress in human endothelial cells and modulates the glutathione redox cycle. Free Radic. Biol. Med. 33, 1527-1533 (2002).
8. O'Malley, Y. Q. et al. The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 285, L1077-1086 (2003).
9. Das, T., Kutty, S. K., Kumar, N., Manefield, M. Pyocyanin Facilitates Extracellular DNA Binding to Pseudomonas aeruginosa Influencing Cell Surface Properties and Aggregation. PLoS ONE 8, e58299 (2013).
10. Gloag, E. S. et al. Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc. Natl. Acad. Sci. U. S. A. 110, 11541-11546 (2013).
11. Barakat, R., Goubet, I., Manon, S., Berges, T., Rosenfeld, E. Unsuspected pyocyanin effect in yeast under anaerobiosis. MicrobiologyOpen 3, 1-14 (2014).
12. Morales, D. K. et al. Control of Candida albicans metabolism and biofilm formation by Pseudomonas aeruginosa phenazines. mBio 4, e00526-00512 (2013).
13. Wang, Y. et al. Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J. Bacteriol. 193, 3606-3617 (2011).
14. Paugam, A. et al. Characteristics and consequences of airway colonization by filamentous fungi in 201 adult patients with cystic fibrosis in France. Med. Mycol.48 Suppl 1, S32-36 (2010).
15. Sudfeld, C. R., Dasenbrook, E. C., Merz, W. G., Carroll, K. C., Boyle, M. P. Prevalence and risk factors for recovery of filamentous fungi in individuals with cystic fibrosis. J. Cyst. Fibros. Off. J. Eur. Cyst. Fibros. Soc. 9, 110-116 (2010).
16. Kerr, J. R. et al. Pseudomonas aeruginosa pyocyanin and 1-hydroxyphenazine inhibit fungal growth. J. Clin. Pathol. 52, 385-387 (1999).
17. Moree, W. J. et al. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 109, 13811-13816 (2012).
18. Lambou, K., Lamarre, C., Beau, R.,Dufour, N., Latge, J.-P. Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol. Microbiol. 75, 910-923 (2010).
19. Paris, S. et al. Catalases of Aspergillus fumigatus. Infect. Immun. 71, 3551-3562 (2003).
20. Lamarre, C., Ibrahim-Granet, O., Du, C., Calderone, R., Latgé, J.-P. Characterization of the SKN7 ortholog of Aspergillus fumigatus. Fungal Genet. Biol. FG B 44, 682-690 (2007).
21. Lessing, F. et al. The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot. Cell 6, 2290-2302 (2007).
22. Haas, H. Iron-A Key Nexus in the Virulence of Aspergillus fumigatus. Front. Microbiol. 3, 28 (2012).
23. Hissen,A.H. T., Chow, J. M. T., Pinto, L. J., Moore, M. M. Survival of Aspergillus fumigatus in Serum Involves Removal of Iron from Transferrin: the Role of Siderophores. Infect. Immun. 72, 1402-1408 (2004).
24. Hissen, A. H. T., Wan, A. N. C., Warwas, M. L., Pinto, L. J., Moore, M. M. The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infect. Immun. 73, 5493-5503 (2005).
25. Schrettl, M. et al. Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J. Exp. Med. 200, 1213-1219 (2004).
26. Hortschansky, P. et al. Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron. EMBO J. 26, 3157-3168 (2007).
27. Schrettl, M. et al. SreA-mediated iron regulation in Aspergillus fumigatus. Mol. Microbiol. 70, 27-43 (2008).
28. Schrettl, M. et al. HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathog. 6, e1001124 (2010).
29. Kropf, D. L. Electrophysiological properties of Achlya hyphae: ionic currents studied by intracellular potential recording. J. Cell Biol. 102, 1209-1216 (1986).
30. Slayman, C. L., Slayman, C. W. Measurement of membrane potentials in Neurospora. Science 136, 876-877 (1962).
31. Brisbane, P. G., Janik, L. J., Tate, M. E., Warren, R. F. Revised structure for the phenazine antibiotic from Pseudomonas fluorescens 2-79 (NRRL B-15132). Antimicrob. Agents Chemother. 31, 1967-1971 (1987).
32. Martnez, M. C.,riantsitohaina, R. Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid. Redox Signal. 11, 669-702 (2009).
33. Deng, T., Xu, K., Zhang, L., Zheng, X. Dynamic determination of Ox-LDLinduced oxidative/nitrosative stress in single macrophage by using fluorescent probes. Cell Biol. Int. 32, 1425-1432 (2008).
34. Doridot, L., Daniel V. F. et al. Nitroso-redox balance and mitochondrial homeostasis are regulated by STOX1, a pre-eclampsia associated gene. Antioxid. Redox Signal. doi:10.1089/ars.2013.5661 (2014).
35. Wang, Y., Newman, D. K. Redox reactions of phenazine antibiotics with ferric (hydr)oxides and molecular oxygen. Environ. Sci. Technol. 42, 2380-2386 (2008).
36. Hassett, D. J., Charniga, L., Bean, K., Ohman, D. E., Cohen, M. S. Response of Pseudomonas aeruginosa to pyocyanin: mechanisms of resistance, antioxidant defenses, and demonstration of a manganese-cofactored superoxide dismutase. Infect. Immun. 60, 328-336 (1992).
37. Chin-A-Woeng, T. F. C., Bloemberg, G. V., Lugtenberg, B. J. J. Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytol. 157, 503-523 (2003).
38. Smallwood, H. S., Shi, L., Squier, T. C. Increases in calmodulin abundance and stabilization of activated inducible nitric oxide synthase mediate bacterial killing in RAW 264.7 macrophages. Biochemistry (Mosc.) 45, 9717-9726 (2006).
39. Fang, F. C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2, 820-832 (2004).
40. Novo, E., Parola, M. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 1, 5 (2008).
41. Hernandez, M. E., Kappler, A., Newman, D. K. Phenazines and other redoxactive antibiotics promote microbial mineral reduction. Appl. Environ. Microbiol. 70, 921-928 (2004).
42. Banin, E., Vasil, M. L., Greenberg, E. P. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 102, 11076-11081 (2005).
43. Hunter, R. C. et al. Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. mBio 4 doi: 10.1128/mBio.00557-13 (2013).
44. Ferreira, M. E., Da. S. et al. The akuBKU80 Mutant Deficient for Nonhomologous End Joining Is a Powerful Tool for Analyzing Pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5, 207-211 (2006).
45. Pontecorvo, G., Roper, J. A., Forbes, E. Genetic Recombination without Sexual Reproduction in Aspergillus niger. J. Gen. Microbiol. 8, 198-210 (1953).
46. Clavaud, C., Beauvais, A., Barbin, L., Munier-Lehmann, H., Latgé, J.-P. The composition of the culture medium influences the b-1,3-glucan metabolism of Aspergillus fumigatus and the antifungal activity of inhibitors of b-1,3-glucan synthesis. Antimicrob. Agents Chemother. 56, 3428-3431 (2012).
47. O'Toole, G. A. Microtiter dish biofilm formation assay. J. Vis. Exp. JoVE. doi:10.3791/2437 (2011).
48. Oberegger, H., Schoeser, M., Zadra, I., Abt, B., Haas, H. SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol. Microbiol. 41, 1077-1089 (2001).