The evolution of alternative biofilms in an opportunistic fungal pathogen: An explanation for how new signal transduction pathways may evolve

Infection, Genetics and Evolution

Volumn 22, Issue , 2014, Pages 235-243

  Soll, David R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Candida albicans; Evolution of biofilms; Pathogenic biofilm; Recruitment in evolution; Sexual biofilm

Indexed keywords

ARTICLE; CANDIDA ALBICANS; EVOLUTION; FUNGAL CELL; FUNGAL STRUCTURES; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS HYPHAE; HOST PATHOGEN INTERACTION; HUMAN; MATING TYPE; MICROBIAL ACTIVITY; MICROBIAL COLONIZATION; MORPHOLOGICAL TRAIT; NONHUMAN; ORGANISM COLONY; PATHOGENIC BIOFILM; PRIORITY JOURNAL; SEXUAL BIOFILM; SIGNAL TRANSDUCTION; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; BIOFILM; CELL STRUCTURE; CYTOLOGY; FUNGAL STRAIN; GENETIC CONSERVATION; MOLECULAR EVOLUTION; MOLECULAR MODEL; REGULATORY MECHANISM; SEXUAL FUNCTION; YEAST CELL;

CANDIDA ALBICANS;

ANTIFUNGAL AGENT; TRANSCRIPTION FACTOR;

CANDIDA ALBICANS; EVOLUTION OF BIOFILMS; PATHOGENIC BIOFILM; RECRUITMENT IN EVOLUTION; SEXUAL BIOFILM;

BIOFILMS; CANDIDA ALBICANS; CELLS, CULTURED; EVOLUTION, MOLECULAR; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, BIOLOGICAL; NEUTROPHILS; SIGNAL TRANSDUCTION;

EID: 84896718616     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.07.013     Document Type: Article

References (57)

1. Anderson J.M., Soll D.R., Greenberg E.P. Unique phenotype of opaque cells in the white-opaque transition of Candida albicans. J. Bacteriol. 1987, 169:5579-5588.
2. Bahn Y.S., Sundstrom P. CAP1, an adenylate cyclase-associated protein gene, regulates bud-hypha transitions, filamentous growth, and cyclic AMP levels and is required for virulence of Candida albicans. J. Bacteriol. 2001, 183:3211-3223.
3. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
4. Daniels K.J., Srikantha T., Lockhart S.R., Pujol C., Soll D.R. Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J. 2006, 25:2240-2252.
5. Diezmann S., Cox C.J., Schonian G., Vilgalys R.J., Mitchell T.G. Phylogeny and evolution of medical species of Candida and related taxa: a multigenic analysis. J. Clin. Microbiol. 2004, 42:5624-5635.
6. Donlan R.M., Costerton J.W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 2002, 15:167-193.
7. Dusane D.H., Nancharaiah Y.V., Venugopalan V.P., Kumar A.R., Zinjarde S.S. Biofilm formation by a biotechnologically important tropical marine yeast isolate, Yarrowia lipolytica NCIM 3589. Water Sci. Technol. 2008, 58:2467-2475.
8. Finkel J.S., Mitchell A.P. Genetic control of Candida albicans biofilm development. Nat. Rev. Microbiol. 2011, 9:109-118.
9. Fitzpatrick D.A., Logue M.E., Stajich J.E., Butler G. A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 2006, 6:99.
10. Hausner M., Wuertz S. High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 1999, 65:3710-3713.
11. Heise B., van der Felden J., Kern S., Malcher M., Bruckner S., Mosch H.U. The TEA transcription factor Tec1 confers promoter-specific gene regulation by Ste12-dependent and -independent mechanisms. Eukaryot. cell 2010, 9:514-531.
12. Hickman M.A., Zeng G., Forche A., Hirakawa M.P., Abbey D., Harrison B.D., Wang Y.M., Su C.H., Bennett R.J., Wang Y., Berman J. The 'obligate diploid' Candida albicans forms mating-competent haploids. Nature 2013, 494:55-59.
13. Huang G., Wang H., Chou S., Nie X., Chen J., Liu H. Bistable expression of WOR1, a master regulator of white-opaque switching in Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12813-12818.
14. Hull C.M., Johnson A.D. Identification of a mating type-like locus in the asexual pathogenic yeast Candida albicans. Science 1999, 285:1271-1275.
15. Jackson A.P., Gamble J.A., Yeomans T., Moran G.P., Saunders D., Harris D., Aslett M., Barrell J.F., Butler G., Citiulo F., Coleman D.C., de Groot P.W., Goodwin T.J., Quail M.A., McQuillan J., Munro C.A., Pain A., Poulter R.T., Rajandream M.A., Renauld H., Spiering M.J., Tivey A., Gow N.A., Barrell B., Sullivan D.J., Berriman M. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res. 2009, 19:2231-2244.
16. Lan C.Y., Newport G., Murillo L.A., Jones T., Scherer S., Davis R.W., Agabian N. Metabolic specialization associated with phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14907-14912.
17. Lane S., Zhou S., Pan T., Dai Q., Liu H. The basic helix-loop-helix transcription factor Cph2 regulates hyphal development in Candida albicans partly via TEC1. Mol. Cell. Biol. 2001, 21:6418-6428.
18. Legrand M., Lephart P., Forche A., Mueller F.M., Walsh T., Magee P.T., Magee B.B. Homozygosity at the MTL locus in clinical strains of Candida albicans: karyotypic rearrangements and tetraploid formation. Mol. Microbiol. 2004, 52:1451-1462.
19. Lin C.H., Kabrawala S., Fox E.P., Nobile C.J., Johnson A.D., Bennett R.J., Magee B.B. Genetic Control of Conventional and Pheromone-Stimulated Biofilm Formation in Candida albicans. PLoS pathogens 2013, 9:e1003305.
20. Lockhart S.R., Pujol C., Daniels K.J., Miller M.G., Johnson A.D., Pfaller M.A., Soll D.R. In Candida albicans, white-opaque switchers are homozygous for mating type. Genetics 2002, 162:737-745.
21. Lockhart S.R., Zhao R., Daniels K.J., Soll D.R. Alpha-pheromone-induced "shmooing" and gene regulation require white-opaque switching during Candida albicans mating. Eukaryot. Cell 2003, 2:847-855.
22. Lohse M.B., Johnson A.D. White-opaque switching in Candida albicans. Curr. Opin. Microbiol. 2009, 12:650-654.
23. Lu Y., Su C., Wang A., Liu H. Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol. 2011, 9:e1001105.
24. Miller M.G., Johnson A.D. White-opaque switching in Candida albicans is controlled by mating-type locus homeodomain proteins and allows efficient mating. Cell 2002, 110:293-302.
25. Morrow B., Srikantha T., Anderson J., Soll D.R. Coordinate regulation of two opaque-phase-specific genes during white-opaque switching in Candida albicans. Infect. Immun. 1993, 61:1823-1828.
26. Morrow B., Srikantha T., Soll D.R. Transcription of the gene for a pepsinogen, PEP1, is regulated by white-opaque switching in Candida albicans. Mol. Cell. Biol. 1992, 12:2997-3005.
27. Morschhäuser J. Regulation of white-opaque switching in Candida albicans. Med. Microbiol. Immunol. 2010, 199:165-172.
28. Nobile C.J., Fox E.P., Nett J.E., Sorrells T.R., Mitrovich Q.M., Hernday A.D., Tuch B.B., Andes D.R., Johnson A.D. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 2012, 148:126-138.
29. Nobile C.J., Nett J.E., Hernday A.D., Homann O.R., Deneault J.S., Nantel A., Andes D.R., Johnson A.D., Mitchell A.P. Biofilm matrix regulation by Candida albicans Zap1. PLoS biology 2009, 7:e1000133.
30. Odds F.C. Candida and candidosis: a review and bibliography 1988, Bailliere Tindall, London, United Kingdom. 2nd ed.
31. Odds F.C., Bougnoux M.E., Shaw D.J., Bain J.M., Davidson A.D., Diogo D., Jacobsen M.D., Lecomte M., Li S.Y., Tavanti A., Maiden M.C., Gow N.A., d'Enfert C. Molecular phylogenetics of Candida albicans. Eukaryot. Cell 2007, 6:1041-1052.
32. Park Y.-N., Daniels K.J., Pujol C., Srikantha T., Soll D.R. Candida albicans forms a specialized "sexual" as well as pathogenic biofilm. Eukaryot. Cell 2013, 12:1120-1131.
33. Pendrak M.L., Yan S.S., Roberts D.D. Hemoglobin regulates expression of an activator of mating-type locus alpha genes in Candida albicans. Eukaryot. Cell 2004, 3:764-775.
34. Piispanen A.E., Bonnefoi O., Carden S., Deveau A., Bassilana M., Hogan D.A. Roles of Ras1 membrane localization during Candida albicans hyphal growth and farnesol response. Eukaryot. Cell 2011, 10:1473-1484.
35. Porman A.M., Alby K., Hirakawa M.P., Bennett R.J. Discovery of a phenotypic switch regulating sexual mating in the opportunistic fungal pathogen Candida tropicalis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:21158-21163.
36. Pujol C., Daniels K.J., Lockhart S.R., Srikantha T., Radke J.B., Geiger J., Soll D.R. The closely related species Candida albicans and Candida dubliniensis can mate. Eukaryot. Cell 2004, 3:1015-1027.
37. Sahni N., Yi S., Daniels K.J., Huang G., Srikantha T., Soll D.R. Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways. PLoS Biol. 2010, 8:e1000363.
38. Sahni N., Yi S., Daniels K.J., Srikantha T., Pujol C., Soll D.R. Genes selectively up-regulated by pheromone in white cells are involved in biofilm formation in Candida albicans. PLoS Pathog. 2009, 5:e1000601.
39. Sahni N., Yi S., Pujol C., Soll D.R. The white cell response to pheromone is a general characteristic of Candida albicans strains. Eukaryot. Cell 2009, 8:251-256.
40. Slutsky B., Staebell M., Anderson J., Risen L., Pfaller M., Soll DR. "White-opaque transition": a second high-frequency switching system in Candida albicans. J. Bacteriol. 1987, 169:189-197.
41. Soll D.R. High-frequency switching in Candida albicans. Clin. Microbiol. rev. 1992, 5:183-203.
42. Soll D.R. Candida and candidosis: Switching and Matin 2011, ASM Press, Washington, D.C. Calderone CCaR (ed.).
43. Srikantha T., Borneman A.R., Daniels K.J., Pujol C., Wu W., Seringhaus M.R., Gerstein M., Yi S., Snyder M., Soll D.R. TOS9 regulates white-opaque switching in Candida albicans. Eukaryot. Cell 2006, 5:1674-1687.
44. Srikantha T., Daniels K.J., Pujol C., Kim E., Soll D.R. Identification of genes upregulated by the transcription factor bcr1 that are involved in impermeability, impenetrability and drug-resistance of Candida albicans a/alpha biofilms. Eukaryot. Cell 2013, 12:875-888.
45. Srikantha T., Daniels K.J., Pujol C., Sahni N., Yi S., Soll D.R. Nonsex genes in the mating type locus of Candida albicans play roles in a/alpha biofilm formation, including impermeability and fluconazole resistance. PLoS Pathog. 2012, 8:e1002476.
46. Srikantha T., Soll D.R. A white-specific gene in the white-opaque switching system of Candida albicans. Gene 1993, 131:53-60.
47. Stewart P.S., Costerton J. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358:135-138.
48. Sudbery P.E. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 2011, 9:737-748.
49. Tavanti A., Davidson A.D., Fordyce M.J., Gow N.A., Maiden M.C., Odds F.C. Population structure and properties of Candida albicans, as determined by multilocus sequence typing. J. Clin. Microbiol. 2005, 43:5601-5613.
50. Uppuluri P., Pierce C.G., Thomas D.P., Bubeck S.S., Saville S.P., Lopez-Ribot J.L. The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot. Cell 2010, 9:1531-1537.
51. Xie J., Tao L., Nobile C.J., Tong Y., Guan G., Sun Y., Cao C., Hernday A.D., Johnson A.D., Zhang L., Bai F.Y., Huang G. White-opaque switching in natural MTLa/alpha isolates of Candida albicans: evolutionary implications for roles in host adaptation, pathogenesis, and sex. PLoS Biol. 2013, 11:e1001525.
52. Yi, S., Sahni, N., Daniels, K.J., Lu, K.L., Huang, G., Garnaas, A.M., Pujol, C., Srikantha, T., Soll, D.R., 2011a. Utilization of the mating scaffold protein in the evolution of a new signal transduction pathway for biofilm development. mBio 2, e00237-00210.
53. Yi S., Sahni N., Daniels K.J., Lu K.L., Huang G., Srikantha T., Soll D.R. Self-induction of a/a or alpha/alpha biofilms in Candida albicans is a pheromone-based paracrine system requiring switching. Eukaryot. Cell 2011, 10:753-760.
54. Yi S., Sahni N., Daniels K.J., Lu K.L., Srikantha T., Huang G., Garnaas A.M., Soll D.R. Alternative mating type configurations (a/alpha versus a/a or alpha/alpha) of Candida albicans result in alternative biofilms regulated by different pathways. PLoS Biol. 2011, 9:e1001117.
55. Yi S., Sahni N., Daniels K.J., Pujol C., Srikantha T., Soll D.R. The same receptor, G protein, and mitogen-activated protein kinase pathway activate different downstream regulators in the alternative white and opaque pheromone responses of Candida albicans. Mol. Biol. Cell 2008, 19:957-970.
56. Yi S., Sahni N., Pujol C., Daniels K.J., Srikantha T., Ma N., Soll D.R. A Candida albicans-specific region of the alpha-pheromone receptor plays a selective role in the white cell pheromone response. Mol. Microbiol. 2009, 71:925-947.
57. Zordan R.E., Galgoczy D.J., Johnson A.D. Epigenetic properties of white-opaque switching in Candida albicans are based on a self-sustaining transcriptional feedback loop. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12807-12812.