Multilocus sequence typing reveals that the population structure of Candida dubliniensis is significantly less divergent than that of Candida albicans

Journal of Clinical Microbiology

Volumn 46, Issue 2, 2008, Pages 652-664

  McManus, Brenda A ^a   Coleman, David C ^a   Moran, Gary ^a   Pinjon, Emmanuelle ^a   Diogo, Dorothée ^b   Bougnoux, Marie Elisabeth ^b   Borecká Melkusova, Silvia ^c   Bujdákova, Helena ^c   Murphy, Philip ^d   D'Enfert, Christophe ^b   Sullivan, Derek J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b INSTITUT PASTEUR   (France)

^c Physics and Informatics   (Slovakia)

^d ADELAIDE AND MEATH HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER;

ARTICLE; CANDIDA ALBICANS; CANDIDA DUBLINIENSIS; CLADISTICS; DNA FINGERPRINTING; GENE CLUSTER; GENE LINKAGE DISEQUILIBRIUM; GENETIC VARIABILITY; GENOTYPE; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENETIC TREE; PHYLOGENY; POPULATION STRUCTURE; PRIORITY JOURNAL; RIBOSOME; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

AMINO ACID SUBSTITUTION; CANDIDA; CANDIDIASIS; CLUSTER ANALYSIS; DNA PRIMERS; DNA, FUNGAL; EPIDEMIOLOGY, MOLECULAR; FUNGAL PROTEINS; GENOTYPE; HUMANS; MYCOLOGICAL TYPING TECHNIQUES; POLYMORPHISM, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

CANDIDA ALBICANS; CANDIDA DUBLINIENSIS;

EID: 38949099749     PISSN: 00951137     EISSN: None     Source Type: Journal    
DOI: 10.1128/JCM.01574-07     Document Type: Article

References (57)

1. Agapow, P. M., and A. Burt. 2001. Indices of multilocus linkage disequilibrium. Mol. Ecol. Notes 1:101-102.
2. Al Mosaid, A., D. Sullivan, I. F. Salkin, D. Shanley, and D. C. Coleman. 2001. Differentiation of Candida dubliniensis from Candida albicans on Staib agar and caffeic acid-ferric citrate agar. J. Clin. Microbiol. 39:323-327.
3. Al Mosaid, A., D. J. Sullivan, and D. C. Coleman. 2003. Differentiation of Candida dubliniensis from Candida albicans on Pal's agar. J. Clin. Microbiol. 41:4787-4789.
4. Al Mosaid, A., D. J. Sullivan, I. Polacheck, F. A. Shaheen, O. Soliman, S. Al Hedaithy, S. Al Thawad, M. Kabadaya, and D. C. Coleman. 2005. Novel 5-flucytosine-resistant clade of Candida dubliniensis from Saudi Arabia and Egypt identified by Cd25 fingerprinting. J. Clin. Microbiol. 43:4026-4036.
5. Bain, J. M., A. Tavanti, A. D. Davidson, M. D. Jacobsen, D. Shaw, N. A. Gow, and F. C. Odds. 2007. Multilocus sequence typing of the pathogenic fungus Aspergillus fumigatus. J. Clin. Microbiol. 45:1469-1477.
6. Blignaut, E., C. Pujol, S. Lockhart, S. Joly, and D. R. Soll. 2002. Ca3 fingerprinting of Candida albicans isolates from human immunodeficiency virus-positive and healthy individuals reveals a new clade in South Africa. J. Clin. Microbiol. 40:826-836.
7. Bougnoux, M. E., D. M. Aanensen, S. Morand, M. Theraud, B. G. Spratt, and C. d'Enfert. 2004. Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect. Genet. Evol. 4:243-252.
8. Bougnoux, M. E., D. Diogo, N. Francois, B. Sendid, S. Veirmeire, J. F. Colombel, C. Bouchier, H. Van Kruiningen, C. d'Enfert, and D. Poulain. 2006. Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J. Clin. Microbiol. 44:1810-1820.
9. Bougnoux, M. E., S. Morand, and C. d'Enfert. 2002. Usefulness of multilocus sequence typing for characterization of clinical isolates of Candida albicans. J. Clin. Microbiol. 40:1290-1297.
10. Bougnoux, M. E., A. Tavanti, C. Bouchier, N. A. Gow, A. Magnier, A. D. Davidson, M. C. Maiden, C. D'Enfert, and F. C. Odds. 2003. Collaborative consensus for optimized multilocus sequence typing of Candida albicans. J. Clin. Microbiol. 41:5265-5266.
11. Boyle, B. M., D. J. Sullivan, C. Forkin, F. Mulcahy, C. T. Keane, and D. C. Coleman. 2002. Candida dubliniensis candidaemia in an HIV-positive patient in Ireland. Int. J. STD AIDS 13:55-57.
12. Buck, J. D. 1990. Isolation of Candida albicans and halophilic Vibrio spp. from aquatic birds in Connecticut and Florida. Appl. Environ. Microbiol. 56:826-828.
13. Bujdakova, H., S. Melkusova, I. Soji, M. Mokras, and Y. Mikami. 2004. Discrimination between Candida albicans and Candida dubliniensis isolated from HIV-positive patients by using commercial method in comparison with PCR assay. Folia Microbiol. (Prague) 49:484-490.
14. Cafarchia, C., A. Camarda, D. Romito, M. Campolo, N. C. Quaglia, D. Tullio, and D. Otranto. 2006. Occurrence of yeasts in cloacae of migratory birds. Mycopathologia 161:229-234.
15. Chan-Tack, K. M. 2005. Fatal Candida dubliniensis septicemia in a patient with AIDS. Clin. Infect. Dis. 40:1209-1210.
16. Chen, K. W., Y. C. Chen, H. J. Lo, F. C. Odds, T. H. Wang, C. Y. Lin, and S. Y. Li. 2006. Multilocus sequence typing for analyses of clonality of Candida albicans strains in Taiwan. J. Clin. Microbiol. 44:2172-2178.
17. Dodgson, A. R., C. Pujol, D. W. Denning, D. R. Soll, and A. J. Fox. 2003. Multilocus sequence typing of Candida glabrata reveals geographically enriched clades. J. Clin. Microbiol. 41:5709-5717.
18. Donnelly, S. M., D. J. Sullivan, D. B. Shanley, and D. C. Coleman. 1999. Phylogenetic analysis and rapid identification of Candida dubliniensis based on analysis of ACT1 intron and exon sequences. Microbiology 145:1871-1882.
19. Fell, J. W. 1993. Rapid identification of yeast species using three primers in a polymerase chain reaction. Mol. Mar. Biol. Biotechnol. 2:174-180.
20. Gallagher, P. J., D. E. Bennett, M. C. Henman, R. J. Russell, S. R. Flint, D. B. Shanley, and D. C. Coleman. 1992. Reduced azole susceptibility of oral isolates of Candida albicans from HIV-positive patients and a derivative exhibiting colony morphology variation. J. Gen. Microbiol. 138:1901-1911.
21. Gee, S. F., S. Joly, D. R. Soll, J. F. Meis, P. E. Verweij, I. Polacheck, D. J. Sullivan, and D. C. Coleman. 2002. Identification of four distinct genotypes of Candida dubliniensis and detection of microevolution in vitro and in vivo. J. Clin. Microbiol. 40:556-574.
22. Gilfillan, G. D., D. J. Sullivan, K. Haynes, T. Parkinson, D. C. Coleman, and N. A. Gow. 1998. Candida dubliniensis: phylogeny and putative virulence factors. Microbiology 144:829-838.
23. Hasenclever, H. F., and R. M. Kogan. 1975. Candida albicans associated with the gastrointestinal tract of the common pigeon (Columbia livia). Sabouraudia 13:116-120.
24. Hunter, P. R. 1990. Reproducibility and indices of discriminatory power of microbial typing methods. J. Clin. Microbiol. 28:1903-1905.
25. Jacobsen, M. D., N. A. Gow, M. C. Maiden, D. J. Shaw, and F. C. Odds. 2007. Strain typing and determination of population structure of Candida krusei by multilocus sequence typing. J. Clin. Microbiol. 45:317-323.
26. Joly, S., C. Pujol, M. Rysz, K. Vargas, and D. R. Soll. 1999. Development and characterization of complex DNA fingerprinting probes for the infectious yeast Candida dubliniensis. J. Clin. Microbiol. 37:1035-1044.
27. Kibbler, C. C., S. Seaton, R. A. Barnes, W. R. Gransden, R. E. Holliman, E. M. Johnson, J. D. Perry, D. J. Sullivan, and J. A. Wilson. 2003. Management and outcome of bloodstream infections due to Candida species in England and Wales. J. Hosp. Infect. 54:18-24.
28. Maiden, M. C., J. A. Bygraves, E. Feil, G. Morelli, J. E. Russell, R. Urwin, Q. Zhang, J. Zhou, K. Zurth, D. A. Caugant, I. M. Feavers, M. Achtman, and B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95:3140-3145.
29. Marriott, D., M. Laxton, and J. Harkness. 2001. Candida dubliniensis candidemia in Australia. Emerg. Infect. Dis. 7:479.
30. McMullan, R., J. Xu, J. E. Moore, B. C. Millar, M. J. Walker, S. T. Irwin, J. Price, J. Barr, and S. Hedderwick. 2002. Candida dubliniensis bloodstream infection in patients with gynaecological malignancy. Eur. J. Clin. Microbiol. Infect. Dis. 21:635-636.
31. Meis, J. F., M. Ruhnke, B. E. De Pauw, F. C. Odds, W. Siegert, and P. E. Verweij. 1999. Candida dubliniensis candidemia in patients with chemotherapy-induced neutropenia and bone marrow transplantation. Emerg. Infect. Dis. 5:150-153.
32. Melkusova, S., M. Lisalova, P. Pavlik, and H. Bujdakova. 2005. The first clinical isolates of Candida dubliniensis in Slovakia. Mycopathologia 159: 369-371.
33. Moran, G., C. Stokes, S. Thewes, B. Hube, D. C. Coleman, and D. Sullivan. 2004. Comparative genomics using Candida albicans DNA microarrays reveals absence and divergence of virulence-associated genes in Candida dubliniensis. Microbiology 150:3363-3382.
34. Nunn, M. A. 2007. Environmental source of Candida dubliniensis. Emerg. Infect. Dis. 13:747-750.
35. Odds, F. C., M. E. Bougnoux, D. J. Shaw, J. M. Bain, A. D. Davidson, D. Diogo, M. D. Jacobsen, M. Lecomte, S. Y. Li, A. Tavanti, M. C. Maiden, N. A. Gow, and C. d'Enfert. 2007. Molecular phylogenetics of Candida albicans. Eukaryot. Cell 6:1041-1052.
36. Odds, F. C., A. D. Davidson, M. D. Jacobsen, A. Tavanti, J. A. Whyte, C. C. Kibbler, D. H. Ellis, M. C. Maiden, D. J. Shaw, and N. A. Gow. 2006. Candida albicans strain maintenance, replacement, and microvariation demonstrated by multilocus sequence typing. J. Clin. Microbiol. 44:3647-3658.
37. Pincus, D. H., D. C. Coleman, W. R. Pruitt, A. A. Padhye, I. F. Salkin, M. Geimer, A. Bassel, D. J. Sullivan, M. Clarke, and V. Hearn. 1999. Rapid identification of Candida dubliniensis with commercial yeast identification systems. J. Clin. Microbiol. 37:3533-3539.
38. Pinjon, E., D. Sullivan, I. Salkin, D. Shanley, and D. Coleman. 1998. Simple, inexpensive, reliable method for differentiation of Candida dubliniensis from Candida albicans. J. Clin. Microbiol. 36:2093-2095.
39. Polacheck, I., J. Strahilevitz, D. Sullivan, S. Donnelly, I. F. Salkin, and D. C. Coleman. 2000. Recovery of Candida dubliniensis from non-human immunodeficiency virus-infected patients in Israel. J. Clin. Microbiol. 38:170-174.
40. Ponton, J., R. Ruchel, K. V. Clemons, D. C. Coleman, R. Grillot, J. Guarro, D. Aldebert, P. Ambroise-Thomas, J. Cano, A. J. Carrillo-Munoz, J. Gene, C. Pinel, D. A. Stevens, and D. J. Sullivan. 2000. Emerging pathogens. Med. Mycol. 38(Suppl. 1):225-236.
41. Pressler, B. M., S. L. Vaden, I. F. Lane, L. D. Cowgill, and J. A. Dye. 2003. Candida spp. urinary tract infections in 13 dogs and seven cats: predisposing factors, treatment, and outcome. J. Am. Anim. Hosp. Assoc. 39:263-270.
42. Pujol, C., M. Pfaller, and D. R. Soll. 2002. Ca3 fingerprinting of Candida albicans bloodstream isolates from the United States, Canada, South America, and Europe reveals a European clade. J. Clin. Microbiol. 40: 2729-2740.
43. Robles, J. C., L. Koreen, S. Park, and D. S. Perlin. 2004. Multilocus sequence typing is a reliable alternative method to DNA fingerprinting for discriminating among strains of Candida albicans. J. Clin. Microbiol. 42:2480-2488.
44. Smith, J. M., N. H. Smith, M. O'Rourke, and B. G. Spratt. 1993. How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90:4384-4388.
45. Soll, D. R. 2000. The ins and outs of DNA fingerprinting the infectious fungi. Clin. Microbiol. Rev. 13:332-370.
46. Soll, D. R., and C. Pujol. 2003. Candida albicans clades. FEMS Immunol. Med. Microbiol. 39:1-7.
47. Stokes, C., G. P. Moran, M. J. Spiering, G. T. Cole, D. C. Coleman, and D. J. Sullivan. 2007. Lower filamentation rates of Candida dubliniensis contribute to its lower virulence in comparison with Candida albicans. Fungal Genet. Biol. 44:920-931.
48. Sullivan, D., K. Haynes, J. Bille, P. Boerlin, L. Rodero, S. Lloyd, M. Henman, and D. Coleman. 1997. Widespread geographic distribution of oral Candida dubliniensis strains in human immunodeficiency virus-infected individuals. J. Clin. Microbiol. 35:960-964.
49. Sullivan, D. J., G. P. Moran, and D. C. Coleman. 2005. Candida dubliniensis: ten years on. FEMS Microbiol. Lett. 253:9-17.
50. Sullivan, D. J., G. P. Moran, E. Pinjon, A. Al-Mosaid, C. Stokes, C. Vaughan, and D. C. Coleman. 2004. Comparison of the epidemiology, drug resistance mechanisms, and virulence of Candida dubliniensis and Candida albicans. FEMS Yeast Res. 4:369-376.
51. Sullivan, D. J., T. J. Westerneng, K. A. Haynes, D. E. Bennett, and D. C. Coleman. 1995. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141:1507-1521.
52. Tavanti, A., A. D. Davidson, M. J. Fordyce, N. A. Gow, M. C. Maiden, and F. C. Odds. 2005. Population structure and properties of Candida albicans, as determined by multilocus sequence typing. J. Clin. Microbiol. 43:5601-5613.
53. Tavanti, A., A. D. Davidson, E. M. Johnson, M. C. Maiden, D. J. Shaw, N. A. Gow, and F. C. Odds. 2005. Multilocus sequence typing for differentiation of strains of Candida tropicalis. J. Clin. Microbiol. 43:5593-5600.
54. Tavanti, A., N. A. Gow, S. Senesi, M. C. Maiden, and F. C. Odds. 2003. Optimization and validation of multilocus sequence typing for Candida albicans. J. Clin. Microbiol. 41:3765-3776.
55. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
56. Vilela, M. M., K. Kamei, A. Sano, R. Tanaka, J. Uno, I. Takahashi, J. Ito, K. Yarita, and M. Miyaji. 2002. Pathogenicity and virulence of Candida dubliniensis: comparison with C. albicans. Med. Mycol. 40:249-257.
57. White, T. J., T. D. Bruns, S. B. Lee, and J. W. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, p. 315-322. In M. A. Innis, D. H. Gelfand, J. J. Sininsky, and T. J. White (ed.), PCR protocols: a guide to methods and applications. Academic Press, Inc., San Diego, CA.