1887

Abstract

(Pa) and (Ca) are major bacterial and fungal pathogens in immunocompromised hosts, and notably in the airways of cystic fibrosis patients. The bacteriophages of Pa physically alter biofilms, and were recently shown to inhibit the biofilms of . To understand the range of this viral–fungal interaction, we studied Pa phages Pf4 and Pf1, and their interactions with Ca biofilm formation and preformed Ca biofilm. Both forms of Ca biofilm development, as well as planktonic Ca growth, were inhibited by either phage. The inhibition of biofilm was reversed by the addition of iron, suggesting that the mechanism of phage action on Ca involves denial of iron. Birefringence studies on added phage showed an ordered structure of binding to Ca. Electron microscopic observations indicated phage aggregation in the biofilm extracellular matrix. Bacteriophage–fungal interactions may be a general feature with several pathogens in the fungal kingdom.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000539
2017-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/11/1568.html?itemId=/content/journal/micro/10.1099/mic.0.000539&mimeType=html&fmt=ahah

References

  1. Williams HD, Davies JC. Basic science for the chest physician: Pseudomonas aeruginosa and the cystic fibrosis airway. Thorax 2012; 67:465–467 [View Article][PubMed]
    [Google Scholar]
  2. Bhargava V, Tomashefski JF, Stern RC, Abramowsky CR. The pathology of fungal infection and colonization in patients with cystic fibrosis. Hum Pathol 1989; 20:977–986 [View Article][PubMed]
    [Google Scholar]
  3. Cimon B, Carrere J, Chazalette JP, Ginies JL, Six P et al. Fungal colonization and immune response to fungi in cystic fibrosis. J Mycol Med 1995; 5:211–216
    [Google Scholar]
  4. Nagano Y, Millar BC, Johnson E, Goldsmith CE, Elborn JS et al. Fungal infections in patients with cystic fibrosis. Rev Med Microbiol 2007; 18:11–16 [View Article]
    [Google Scholar]
  5. Horré R, Symoens F, Delhaes L, Bouchara JP. Fungal respiratory infections in cystic fibrosis: a growing problem. Med Mycol 2010; 48:S1–S3 [View Article][PubMed]
    [Google Scholar]
  6. Middleton PG, Chen SC, Meyer W. Fungal infections and treatment in cystic fibrosis. Curr Opin Pulm Med 2013; 19:670–675 [View Article][PubMed]
    [Google Scholar]
  7. Anand R, Moss RB, Sass G, Banaei N, Clemons KV et al. Small colony variants of Pseudomonas aeruginosa display heterogeneity in inhibiting Aspergillus fumigatus biofilm. Mycopathologia 2017 (In press) [View Article][PubMed]
    [Google Scholar]
  8. Hogan DA, Kolter R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 2002; 296:2229–2232 [View Article][PubMed]
    [Google Scholar]
  9. Hogan DA, Vik A, Kolter R. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 2004; 54:1212–1223 [View Article][PubMed]
    [Google Scholar]
  10. Holcombe LJ, Mcalester G, Munro CA, Enjalbert B, Brown AJ et al. Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans . Microbiology 2010; 156:1476–1486 [View Article][PubMed]
    [Google Scholar]
  11. Hall RA, Turner KJ, Chaloupka J, Cottier F, de Sordi L et al. The quorum-sensing molecules farnesol/homoserine lactone and dodecanol operate via distinct modes of action in Candida albicans . Eukaryot Cell 2011; 10:1034–1042 [View Article][PubMed]
    [Google Scholar]
  12. Bandara HM, K Cheung BP, Watt RM, Jin LJ, Samaranayake LP. Pseudomonas aeruginosa lipopolysaccharide inhibits Candida albicans hyphae formation and alters gene expression during biofilm development. Mol Oral Microbiol 2013; 28:54–69 [View Article][PubMed]
    [Google Scholar]
  13. Singh N, Pemmaraju SC, Pruthi PA, Cameotra SS, Pruthi V. Candida biofilm disrupting ability of di-rhamnolipid (RL-2) produced from Pseudomonas aeruginosa DSVP20. Appl Biochem Biotechnol 2013; 169:2374–2391 [View Article][PubMed]
    [Google Scholar]
  14. Tupe SG, Kulkarni RR, Shirazi F, Sant DG, Joshi SP et al. Possible mechanism of antifungal phenazine-1-carboxamide from Pseudomonas sp. against dimorphic fungi Benjaminiella poitrasii and human pathogen Candida albicans . J Appl Microbiol 2015; 118:39–48 [View Article][PubMed]
    [Google Scholar]
  15. Lopez-Medina E, Fan D, Coughlin LA, Ho EX, Lamont IL et al. Candida albicans Inhibits Pseudomonas aeruginosa virulence through suppression of pyochelin and pyoverdine biosynthesis. PLoS Pathog 2015; 11:e1005129 [View Article][PubMed]
    [Google Scholar]
  16. Secor PR, Sweere JM, Michaels LA, Malkovskiy AV, Lazzareschi D et al. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 2015; 18:549–559 [View Article][PubMed]
    [Google Scholar]
  17. Penner JC, Ferreira JA, Secor PR, Sweere JM, Birukova MK et al. Pf4 bacteriophage produced by Pseudomonas aeruginosa inhibits Aspergillus fumigatus metabolism via iron sequestration. Microbiology 2016; 162:1583–1594 [View Article][PubMed]
    [Google Scholar]
  18. Noni M, Katelari A, Kaditis A, Theochari I, Lympari I et al. Candida albicans chronic colonisation in cystic fibrosis may be associated with inhaled antibiotics. Mycoses 2015; 58:416–421 [View Article][PubMed]
    [Google Scholar]
  19. Chotirmall SH, O'Donoghue E, Bennett K, Gunaratnam C, O'Neill SJ et al. Sputum Candida albicans presages FEV1 decline and hospital-treated exacerbations in cystic fibrosis. Chest 2010; 138:1186–1195 [View Article][PubMed]
    [Google Scholar]
  20. Gileles-Hillel A, Shoseyov D, Polacheck I, Korem M, Kerem E et al. Association of chronic Candida albicans respiratory infection with a more severe lung disease in patients with cystic fibrosis. Pediatr Pulmonol 2015; 50:1082–1089 [View Article][PubMed]
    [Google Scholar]
  21. Liu M, Clemons KV, Johansen ME, Martinez M, Chen V et al. Saccharomyces as a vaccine against systemic candidiasis. Immunol Invest 2012; 41:847–855 [View Article][PubMed]
    [Google Scholar]
  22. Ramage G, Vandewalle K, Bachmann SP, Wickes BL, López-Ribot JL. In vitro pharmacodynamic properties of three antifungal agents against preformed Candida albicans biofilms determined by time-kill studies. Antimicrob Agents Chemother 2002; 46:3634–3636 [View Article][PubMed]
    [Google Scholar]
  23. Li X, Yan Z, Xu J. Quantitative variation of biofilms among strains in natural populations of Candida albicans . Microbiology 2003; 149:353–362 [View Article][PubMed]
    [Google Scholar]
  24. Kuhn DM, Balkis M, Chandra J, Mukherjee PK, Ghannoum MA. Uses and limitations of the XTT assay in studies of Candida growth and metabolism. J Clin Microbiol 2003; 41:506–508 [View Article][PubMed]
    [Google Scholar]
  25. Chandra J, Mukherjee PK, Ghannoum MA. In vitro growth and analysis of Candida biofilms. Nat Protoc 2008; 3:1909–1924 [View Article][PubMed]
    [Google Scholar]
  26. Pierce CG, Uppuluri P, Tristan AR, Wormley FL, Mowat E et al. A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 2008; 3:1494–1500 [View Article][PubMed]
    [Google Scholar]
  27. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E et al. Comprehensive transposon mutant library of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2003; 100:14339–14344 [View Article][PubMed]
    [Google Scholar]
  28. Boulanger P. Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol Biol 2009; 502:227-38 [View Article][PubMed]
    [Google Scholar]
  29. Hmelo LR, Borlee BR, Almblad H, Love ME, Randall TE et al. Precision-engineering the Pseudomonas aeruginosa genome with two-step allelic exchange. Nat Protoc 2015; 10:1820–1841 [View Article][PubMed]
    [Google Scholar]
  30. Castang S, Dove SL. Basis for the essentiality of H-NS family members in Pseudomonas aeruginosa . J Bacteriol 2012; 194:5101–5109 [View Article][PubMed]
    [Google Scholar]
  31. Anand R, Clemons KV, Stevens DA. Effect of anaerobiasis or hypoxia on Pseudomonas aeruginosa Inhibition of Aspergillus fumigatus Biofilm. Arch Microbiol 2017; 199:881–890 [View Article][PubMed]
    [Google Scholar]
  32. Ferreira JA, Penner JC, Moss RB, Haagensen JA, Clemons KV et al. Inhibition of Aspergillus fumigatus and its biofilm by Pseudomonas aeruginosa is dependent on the source, phenotype and growth conditions of the bacterium. PLoS One 2015; 10:e0134692 [View Article][PubMed]
    [Google Scholar]
  33. Glazer AM, Lewis JG, Kaminsky W. An automatic optical imaging system for birefringent media. Proc R Soc Lond A 1996; 452:2751–2765 [View Article]
    [Google Scholar]
  34. Costerton JW. Anaerobic biofilm infections in cystic fibrosis. Mol Cell 2002; 10:699–700 [View Article][PubMed]
    [Google Scholar]
  35. Yoon SS, Hennigan RF, Hilliard GM, Ochsner UA, Parvatiyar K et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 2002; 3:593–603[PubMed] [Crossref]
    [Google Scholar]
  36. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002; 109:317–325 [View Article][PubMed]
    [Google Scholar]
  37. Werner E, Roe F, Bugnicourt A, Franklin MJ, Heydorn A et al. Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2004; 70:6188–6196 [View Article][PubMed]
    [Google Scholar]
  38. Lambiase A, Catania MR, Rossano F. Anaerobic bacteria infection in cystic fibrosis airway disease. New Microbiol 2010; 33:185–194[PubMed]
    [Google Scholar]
  39. Cowley ES, Kopf SH, Lariviere A, Ziebis W, Newman DK. Pediatric cystic fibrosis sputum can be chemically dynamic, anoxic, and extremely reduced due to hydrogen sulfide formation. MBio 2015; 6:e00767 [View Article][PubMed]
    [Google Scholar]
  40. Nazik H, Penner JC, Ferreira JA, Haagensen JA, Cohen K et al. Effects of iron chelators on the formation and development of Aspergillus fumigatus biofilm. Antimicrob Agents Chemother 2015; 59:6514–6520 [View Article][PubMed]
    [Google Scholar]
  41. Dogic Z, Fraden S. Ordered phases of filamentous viruses. Curr Opin Colloid Interface Sci 2006; 11:47–55 [View Article]
    [Google Scholar]
  42. Secor PR, Michaels LA, Smigiel KS, Rohani MG, Jennings LK et al. Filamentous bacteriophage produced by Pseudomonas aeruginosa alters the inflammatory response and promotes noninvasive infection in vivo . Infect Immun 2017; 85:e00648-16 [View Article][PubMed]
    [Google Scholar]
  43. Noble SM. Candida albicans specializations for iron homeostasis: from commensalism to virulence. Curr Opin Microbiol 2013; 16:708–715 [View Article][PubMed]
    [Google Scholar]
  44. Schrettl M, Haas H. Iron homeostasis—Achilles' heel of Aspergillus fumigatus?. Curr Opin Microbiol 2011; 14:400–405 [View Article][PubMed]
    [Google Scholar]
  45. Nguyen AT, Oglesby-Sherrouse AG. Spoils of war: iron at the crux of clinical and ecological fitness of Pseudomonas aeruginosa . Biometals 2015; 28:433–443 [View Article][PubMed]
    [Google Scholar]
  46. Tejedor C, Foulds J, Zasloff M. Bacteriophages in sputum of patients with bronchopulmonary Pseudomonas infections. Infect Immun 1982; 36:440–441[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000539
Loading
/content/journal/micro/10.1099/mic.0.000539
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error