Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3696-3704

  Bamford, Caroline V ^a   D'Mello, Anita ^a   Nobbs, Angela H ^a   Dutton, Lindsay C ^a   Vickerman, M Margaret ^b   Jenkinson, Howard F ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CEK1P ENZYME; FARNESOL; HOG1P ENZYME; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MKC1P ENZYME; PROTEIN SSPA; PROTEIN SSPB; S RIBOSYLHOMOCYSTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL CONTACT; CONTROLLED STUDY; ENZYME ACTIVATION; FUNGUS HYPHAE; MICROBIAL ADHESION; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; STREPTOCOCCUS GORDONII;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CANDIDA ALBICANS; CARBON-SULFUR LYASES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FUNGAL PROTEINS; HYPHAE; MITOGEN-ACTIVATED PROTEIN KINASE 3; SIGNAL TRANSDUCTION; STREPTOCOCCUS GORDONII;

EID: 69049120315     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00438-09     Document Type: Article

References (71)

1. Alem, M. A., M. D. Oteef, T. H. Flowers, and L. J. Douglas.2006. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot. Cell 5:1770-1779.
2. Alonso-Monge, R., F. Navarro-Garcia, G. Molero, R. Diez-Orejas, M. Gustin, J. Pla, M. Sanchez, and C. Nombela.1999. Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 181:3058-3068.
3. Bahn, Y. S., M. Molenda, J. F. Staab, C. A. Lyman, L. J. Gordon, and P. Sundstrom.2007. Genome-wide transcriptional profiling of the cyclic AMP-dependent signaling pathway during morphogenic transitions of Candida albicans. Eukaryot. Cell 6:2376-2390.
4. Baillie, G. S., and L. J. Douglas.1999. Role of dimorphism in the development of Candida albicans biofilms. J. Med. Microbiol. 48:671-679.
5. Barnard, J. P., and M. W. Stinson.1996. The alpha-hemolysin of Streptococcus gordonii is hydrogen peroxide. Infect. Immun. 64:3853-3857.
6. Bauernfeind, A., R. M. Bertele, K. Harms, G. Horl, R. Jungwirth, C. Petermuller, B. Przyklenk, and C. Weisslein-Pfister.1987. Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 15:270-277.
7. Biswas, S., D. P. Van, and A. Datta.2007. Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol. Mol. Biol. Rev. 71:348-376.
8. Boon, C., Y. Deng, L. H. Wang, Y. He, J. L. Xu, Y. Fan, S. Q. Pan, and L. H. Zhang.2008. A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J. 2:27-36.
9. Campos, M. S., L. Marchini, L. A. Bernardes, L. C. Paulino, and F. G. Nobrega.2008. Biofilm microbial communities of denture stomatitis. Oral Microbiol. Immunol. 23:419-424.
10. Chandra, J., D. M. Kuhn, P. K. Mukherjee, L. L. Hoyer, T. McCormick, and M. A. Ghannoum.2001. Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183:5385-5394.
11. Chen, H., M. Fujita, Q. Feng, J. Clardy, and G. R. Fink.2004. Tyrosol is a quorum-sensing molecule in Candida albicans. Proc. Natl. Acad. Sci. USA 101:5048-5052.
12. Csank, C., K. Schroppel, E. Leberer, D. Harcus, O. Mohamed, S. Meloche, D. Y. Thomas, and M. Whiteway.1998. Roles of the Candida albicans mitogen-activated protein kinase homolog, Cek1p, in hyphal development and systemic candidiasis. Infect. Immun. 66:2713-2721.
13. Daep, C. A., R. J. Lamont, and D. R. Demuth.2008. Interaction of Porphyromonas gingivalis with oral streptococci requires a motif that resembles the eukaryotic nuclear receptor box protein-protein interaction domain. Infect. Immun. 76:3273-3280.
14. Davis-Hanna, A., A. E. Piispanen, L. I. Stateva, and D. A. Hogan.2008. Farnesol and dodecanol effects on the Candida albicans Ras1-cAMP signalling pathway and the regulation of morphogenesis. Mol. Microbiol. 67:47-62.
15. De Keersmaecker, S. C., K. Sonck, and J. Vanderleyden.2006. Let LuxS speak up in AI-2 signaling. Trends Microbiol. 14:114-119.
16. Egland, P. G., L. D. Du, and P. E. Kolenbrander.2001. Identification of independent Streptococcus gordonii SspA and SspB functions in coaggregation with Actinomyces naeslundii. Infect. Immun. 69:7512-7516.
17. Enjalbert, B., A. Nantel, and M. Whiteway.2003. Stress-induced gene expression in Candida albicans: absence of a general stress response. Mol. Biol. Cell 14:1460-1467.
18. Enjalbert, B., D. A. Smith, M. J. Cornell, I. Alam, S. Nicholls, A. J. Brown, and J. Quinn.2006. Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol. Biol. Cell 17:1018-1032.
19. Enjalbert, B., and M. Whiteway.2005. Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot. Cell 4:1203-1210.
20. Garcia-Sanchez, S., S. Aubert, I. Iraqui, G. Janbon, J. M. Ghigo, and C. d'Enfert.2004. Candida albicans biofilms: a developmental state associated with specific and stable gene expression patterns. Eukaryot. Cell 3:536-545.
21. Geier, H., S. Mostowy, G. A. Cangelosi, M. A. Behr, and T. E. Ford.2008. Autoinducer-2 triggers the oxidative stress response in Mycobacterium avium, leading to biofilm formation. Appl. Environ. Microbiol. 74:1798-1804.
22. Gibson, J., A. Sood, and D. A. Hogan.2009. Pseudomonas aeruginosa-Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl. Environ. Microbiol. 75:504-513.
23. Gow, N. A., A. J. Brown, and F. C. Odds.2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5:366-371.
24. Heddle, C., A. H. Nobbs, N. S. Jakubovics, M. Gal, J. P. Mansell, D. Dymock, and H. F. Jenkinson.2003. Host collagen signal induces antigen I/II adhesin and invasin gene expression in oral Streptococcus gordonii. Mol. Microbiol. 50:597-607.
25. Hogan, D. A., A. Vik, and R. Kolter.2004. A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol. Microbiol. 54:1212-1223.
26. Holmes, A. R., C. Gilbert, J. M. Wells, and H. F. Jenkinson.1998. Binding properties of Streptococcus gordonii SspA and SspB (antigen I/II family) polypeptides expressed on the cell surface of Lactococcus lactis MG1363. Infect. Immun. 66:4633-4639.
27. Holmes, A. R., P. K. Gopal, and H. F. Jenkinson.1995. Adherence of Candida albicans to a cell surface polysaccharide receptor on Streptococcus gordonii. Infect. Immun. 63:1827-1834.
28. Holmes, A. R., R. McNab, and H. F. Jenkinson.1996. Candida albicans binding to the oral bacterium Streptococcus gordonii involves multiple adhesin-receptor interactions. Infect. Immun. 64:4680-4685.
29. Hornby, J. M., E. C. Jensen, A. D. Lisec, J. J. Tasto, B. Jahnke, R. Shoemaker, P. Dussault, and K. W. Nickerson.2001. Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl. Environ. Microbiol. 67:2982-2992.
30. Jakubovics, N. S., S. W. Kerrigan, A. H. Nobbs, N. Stromberg, C. J. van Dolleweerd, D. M. Cox, C. G. Kelly, and H. F. Jenkinson.2005. Functions of cell surface-anchored antigen I/II family and Hsa polypeptides in interactions of Streptococcus gordonii with host receptors. Infect. Immun. 73:6629-6638.
31. Jakubovics, N. S., N. Stromberg, C. J. van Dolleweerd, C. G. Kelly, and H. F. Jenkinson.2005. Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Mol. Microbiol. 55:1591-1605.
32. Jenkinson, H. F., and D. R. Demuth.1997. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol. Microbiol. 23:183-190.
33. Jenkinson, H. F., and L. J. Douglas.2002. Interactions between Candida species and bacteria in mixed infections, p. 357-373. In K. A. Brogden and J. M. Guthmiller (ed.), Polymicrobial diseases. ASM Press, Washington, DC.
34. Jenkinson, H. F., H. C. Lala, and M. G. Shepherd.1990. Coaggregation of Streptococcus sanguis and other streptococci with Candida albicans. Infect. Immun. 58:1429-1436.
35. Jenkinson, H. F., and R. J. Lamont.1997. Streptococcal adhesion and colonization. Crit. Rev. Oral Biol. Med. 8:175-200.
36. Kerrigan, S. W., N. S. Jakubovics, C. Keane, P. Maguire, K. Wynne, H. F. Jenkinson, and D. Cox.2007. Role of Streptococcus gordonii surface proteins SspA/SspB and Hsa in platelet function. Infect. Immun. 75:5740-5747.
37. 2 sensing with cAMP signaling and virulence. Curr. Biol. 15:2021-2026.
38. Kolenbrander, P. E., R. N. Andersen, D. S. Blehert, P. G. Egland, J. S. Foster, and R. J. Palmer, Jr.2002. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66:486-505.
39. Kruppa, M.2009. Quorum sensing and Candida albicans. Mycoses 52:1-10.
40. Kruppa, M., B. P. Krom, N. Chauhan, A. V. Bambach, R. L. Cihlar, and R. A. Calderone.2004. The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryot. Cell 3:1062-1065.
41. Kumamoto, C. A.2005. A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. USA 102:5576-5581.
42. Kumamoto, C. A.2008. Molecular mechanisms of mechanosensing and their roles in fungal contact sensing. Nat. Rev. Microbiol. 6:667-673.
43. Kumamoto, C. A., and M. D. Vinces.2005. Alternative Candida albicans lifestyles: growth on surfaces. Annu. Rev. Microbiol. 59:113-133.
44. Kuramitsu, H. K., X. He, R. Lux, M. H. Anderson, and W. Shi.2007. Interspecies interactions within oral microbial communities. Microbiol. Mol. Biol. Rev. 71:653-670.
45. Lamont, R. J., A. El-Sabaeny, Y. Park, G. S. Cook, J. W. Costerton, and D. R. Demuth.2002. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148:1627-1636.
46. Li, Y. H., N. Tang, M. B. Aspiras, P. C. Lau, J. H. Lee, R. P. Ellen, and D. G. Cvitkovitch.2002. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184:2699-2708.
47. McAlester, G., F. O'Gara, and J. P. Morrissey.2008. Signal-mediated interactions between Pseudomonas aeruginosa and Candida albicans. J. Med. Microbiol. 57:563-569.
48. McNab, R., S. K. Ford, A. El-Sabaeny, B. Barbieri, G. S. Cook, and R. J. Lamont.2003. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185:274-284.
49. Mitchell, A. P.1998. Dimorphism and virulence in Candida albicans. Curr. Opin. Microbiol. 1:687-692.
50. Monge, R. A., E. Roman, C. Nombela, and J. Pla.2006. The MAP kinase signal transduction network in Candida albicans. Microbiology 152:905-912.
51. Murillo, L. A., G. Newport, C. Y. Lan, S. Habelitz, J. Dungan, and N. M. Agabian.2005. Genome-wide transcription profiling of the early phase of biofilm formation by Candida albicans. Eukaryot. Cell 4:1562-1573.
52. Nasution, O., K. Srinivasa, M. Kim, Y. J. Kim, W. Kim, W. Jeong, and W. Choi.2008. Hydrogen peroxide induces hyphal differentiation in Candida albicans. Eukaryot. Cell 7:2008-2011.
53. Navarro-Garcia, F., R. Alonso-Monge, H. Rico, J. Pla, R. Sentandreu, and C. Nombela.1998. A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 144:411-424.
54. Navarro-Garcia, F., B. Eisman, S. M. Fiuza, C. Nombela, and J. Pla.2005. The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 151:2737-2749.
55. Nobbs, A. H., B. H. Shearer, M. Drobni, M. A. Jepson, and H. F. Jenkinson. 2007. Adherence and internalization of Streptococcus gordonii by epithelial cells involves beta1 integrin recognition by SspA and SspB (antigen I/II family) polypeptides. Cell. Microbiol. 9:65-83.
56. Nobile, C. J., and A. P. Mitchell.2006. Genetics and genomics of Candida albicans biofilm formation. Cell. Microbiol. 8:1382-1391.
57. Odds, F. C.1988. Candida and candidosis, 2nd ed. Bailliere Tindall, London, United Kingdom.
58. Paster, B. J., I. Olsen, J. A. Aas, and F. E. Dewhirst.2006. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42:80-87.
59. Podbielski, A., and B. Kreikemeyer.2004. Cell density-dependent regulation: basic principles and effects on the virulence of Gram-positive cocci. Int. J. Infect. Dis. 8:81-95.
60. Ramage, G., S. P. Saville, B. L. Wickes, and J. L. Lopez-Ribot.2002. Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl. Environ. Microbiol. 68:5459-5463.
61. Ramage, G., K. Tomsett, B. L. Wickes, J. L. Lopez-Ribot, and S. W. Redding. 2004. Denture stomatitis: a role for Candida biofilms. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 98:53-59.
62. Rickard, A. H., R. J. Palmer, Jr., D. S. Blehert, S. R. Campagna, M. F. Semmelhack, P. G. Egland, B. L. Bassler, and P. E. Kolenbrander.2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60:1446-1456.
63. Roman, E., D. M. Arana, C. Nombela, R. onso-Monge, and J. Pla.2007. MAP kinase pathways as regulators of fungal virulence. Trends Microbiol. 15:181-190.
64. Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler.2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41:463-476.
65. Shchepin, R., J. M. Hornby, E. Burger, T. Niessen, P. Dussault, and K. W. Nickerson.2003. Quorum sensing in Candida albicans: probing farnesol's mode of action with 40 natural and synthetic farnesol analogs. Chem. Biol. 10:743-750.
66. Smith, D. A., S. Nicholls, B. A. Morgan, A. J. Brown, and J. Quinn.2004. A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol. Biol. Cell 15:4179-4190.
67. Venkatesh, M. P., D. Pham, M. Fein, L. Kong, and L. E. Weisman.2007. Neonatal coinfection model of coagulase-negative Staphylococcus (Staphylococcus epidermidis) and Candida albicans: fluconazole prophylaxis enhances survival and growth. Antimicrob. Agents Chemother. 51:1240-1245.
68. Whiteway, M., and C. Bachewich.2007. Morphogenesis in Candida albicans. Annu. Rev. Microbiol. 61:529-553.
69. Yeater, K. M., J. Chandra, G. Cheng, P. K. Mukherjee, X. Zhao, S. L. Rodriguez-Zas, K. E. Kwast, M. A. Ghannoum, and L. L. Hoyer.2007. Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153:2373-2385.
70. Yoshida, Y., R. J. Palmer, J. Yang, P. E. Kolenbrander, and J. O. Cisar. 2006. Streptococcal receptor polysaccharides: recognition molecules for oral biofilm formation. BMC Oral Health 6:S12.
71. Zhang, Y., Y. Lei, A. Nobbs, A. Khammanivong, and M. C. Herzberg.2005. Inactivation of Streptococcus gordonii SspAB alters expression of multiple adhesin genes. Infect. Immun. 73:3351-3357.