Using a Multi-Locus Microsatellite Typing method improved phylogenetic distribution of Candida albicans isolates but failed to demonstrate association of some genotype with the commensal or clinical origin of the isolates

Infection, Genetics and Evolution

Volumn 12, Issue 8, 2012, Pages 1949-1957

  L'Ollivier, Coralie ^a,b,c   Labruère, Catherine ^d   Jebrane, Ahmed ^d   Bougnoux, Marie Elisabeth ^e,f,g   d'Enfert, Christophe ^e,f   Bonnin, Alain ^a,b,c   Dalle, Frédéric ^a,b,c  

^a DIJON UNIVERSITY HOSPITAL   (France)

^b UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^c UNIVERSITÉ DE BOURGOGNE   (France)

^d UNIVERSITÉ DE BOURGOGNE   (France)

^e INSTITUT PASTEUR   (France)

^f INRA F 75015   (France)

^g UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Allelic frequencies; Candida albicans; Genotyping; Lineages; MLMT; Pathogenicity

Indexed keywords

ARTICLE; CANDIDA ALBICANS; CELL LINEAGE; CLADISTICS; COMMENSAL; CONTROLLED STUDY; DNA ISOLATION; DNA POLYMORPHISM; FUNGAL STRAIN; FUNGUS ISOLATION; GENE AMPLIFICATION; GENE CLUSTER; GENE FREQUENCY; GENE LOCUS; GENETIC ANALYSIS; GENOTYPE; HUMAN; MICROSATELLITE MARKER; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; POPULATION STRUCTURE; PRIORITY JOURNAL; VIRAL GENETICS; VIRUS VIRULENCE;

CANDIDA ALBICANS; CANDIDIASIS; CARRIER STATE; CASE-CONTROL STUDIES; DNA, FUNGAL; GENES, FUNGAL; GENETIC MARKERS; HUMANS; MICROSATELLITE REPEATS; MYCOLOGICAL TYPING TECHNIQUES; PHYLOGENY;

CANDIDA ALBICANS;

EID: 84867118273     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2012.07.025     Document Type: Article

References (72)

1. Adachi H., Shimizu K., Hattori H., Tanaka R., Chibana H., Takagi Y., Tomita Y., Kanbe T. Genotyping of Candida albicans by fragment analysis of microsatellites combined with 25S rDNA and RPS-based strategies. Nihon Ishinkin Gakkai Zasshi 2009, 50:167-174.
2. Awadalla P., Ritland K. Microsatellite variation and evolution in the Mimulus guttatus species complex with contrasting mating systems. Mol. Biol. Evol. 1997, 14:1023-1034.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B 1995, 57:289-300.
4. Bert T.M., Seyoum S., Tringali M.D., McMillen-Jackson A. Methodologies for conservation assessments of the genetic biodiversity of aquatic macro-organisms. Braz. J. Biol. 2002, 62:387-408.
5. Blignaut E., Pujol C., Lockhart S., Joly S., Soll D.R. Ca3 Fingerprinting of Candida albicans isolates from human immunodeficiency virus-positive and healthy individuals reveals a new clade in South Africa. J. Clin. Microbiol. 2002, 40:826-836.
6. Botterel F., Desterke C., Costa C., Bretagne S. Analysis of microsatellite markers of Candida albicans used for rapid typing. J. Clin. Microbiol. 2001, 39:4076-4081.
7. Bougnoux M.E., Aanensen D.M., Morand S., Theraud M., Spratt B.G., d'Enfert C. Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect. Genet. Evol. 2004, 4:243-252.
8. Bougnoux M.E., Diogo D., Francois N., Sendid B., Veirmeire S., Colombel J.F., Bouchier C., Van Kruiningen H., d'Enfert C., Poulain D. Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J. Clin. Microbiol. 2006, 44:1810-1820.
9. Bougnoux M.E., Kac G., Aegerter P., d'Enfert C., Fagon J.Y. Candidemia and candiduria in critically ill patients admitted to intensive care units in France: incidence, molecular diversity, management and outcome. Intensive Care Med. 2008, 34:292-299.
10. Bougnoux M.E., Pujol C., Diogo D., Bouchier C., Soll D.R., d'Enfert C. Mating is rare within as well as between clades of the human pathogen Candida albicans. Fungal Genet. Biol. 2008, 45:221-231.
11. Bougnoux M.E., Tavanti A., Bouchier C., Gow N.A., Magnier A., Davidson A.D., Maiden M.C., D'Enfert C., Odds F.C. Collaborative consensus for optimized multilocus sequence typing of Candida albicans. J. Clin. Microbiol. 2003, 41:5265-5266.
12. Bowcock A.M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J.R., Cavalli-Sforza L.L. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 1994, 368:455-457.
13. Bretagne S., Costa J.M., Besmond C., Carsique R., Calderone R. Microsatellite polymorphism in the promoter sequence of the elongation factor 3 gene of Candida albicans as the basis for a typing system. J. Clin. Microbiol. 1997, 35:1777-1780.
14. Calderone R., Gow N. Host recognition by Candida species 2002, ASM Press, Washington, DC.
15. Calderone R.A., Fonzi W.A. Virulence factors of Candida albicans. Trends Microbiol. 2001, 9:327-335.
16. Charles P.E., Dalle F., Aho S., Quenot J.P., Doise J.M., Aube H., Olsson N.O., Blettery B. Serum procalcitonin measurement contribution to the early diagnosis of candidemia in critically ill patients. Intensive Care Med. 2006, 32:1577-1583.
17. Chavez-Galarza J., Pais C., Sampaio P. Microsatellite typing identifies the major clades of the human pathogen Candida albicans. Infect. Genet. Evol. 2010, 10:697-702.
18. Chowdhary A., Lee-Yang W., Lasker B.A., Brandt M.E., Warnock D.W., Arthington-Skaggs B.A. Comparison of multilocus sequence typing and Ca3 fingerprinting for molecular subtyping epidemiologically-related clinical isolates of Candida albicans. Med. Mycol. 2006, 44:405-417.
19. Cole G.T., Halawa A.A., Anaissie E.J. The role of the gastrointestinal tract in hematogenous candidiasis: from the laboratory to the bedside. Clin. Infect. Dis. 1996, 22(Suppl. 2):S73-S88.
20. Dalle F., Dumont L., Franco N., Mesmacque D., Caillot D., Bonnin P., Moiroux C., Vagner O., Cuisenier B., Aho S., Lizard S., Bonnin A. Genotyping of Candida albicans oral strains from healthy individuals by polymorphic microsatellite locus analysis. J. Clin. Microbiol. 2003, 41.
21. Dalle F., Franco N., Lopez J., Vagner O., Caillot D., Chavanet P., Cuisenier B., Aho S., Lizard S., Bonnin A. Comparative genotyping of Candida albicans bloodstream and nonbloodstream isolates at a polymorphic microsatellite locus. J. Clin. Microbiol. 2000, 38:4554-4559.
22. Dalle F., Lafon I., L'Ollivier C., Ferrant E., Sicard P., Labruere C., Jebrane A., Laubriet A., Vagner O., Caillot D., Bonnin A. A prospective analysis of the genotypic diversity and dynamics of the Candida albicans colonizing flora in neutropenic patients with de novo acute leukemia. Haematologica 2008, 93:581-587.
23. Devlin B., Risch N., Roeder K. No excess of homozygosity at loci used for DNA fingerprinting. Science 1990, 249:1416-1420.
24. Estoup A., Jarne P., Cornuet J.M. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol. Ecol. 2002, 11:1591-1604.
25. Field D., Eggert L., Metzgar D., Rose R., Wills C. Use of polymorphic short and clustered coding-region microsatellites to distinguish strains of Candida albicans. FEMS Immunol. Med. Microbiol. 1996, 15:73-79.
26. Fundyga R.E., Lott T.J., Arnold J. Population structure of Candida albicans, a member of the human flora, as determined by microsatellite loci. Infect. Genet. Evol. 2002, 2:57-68.
27. Garcia-Hermoso D., Cabaret O., Lecellier G., Desnos-Ollivier M., Hoinard D., Raoux D., Costa J.M., Dromer F., Bretagne S. Comparison of microsatellite length polymorphism and multilocus sequence typing for DNA-Based typing of Candida albicans. J. Clin. Microbiol. 2007, 45:3958-3963.
28. Goodman S.J. Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol. Biol. Evol. 1998, 15:104-118.
29. Gow N.A., Brown A.J., Odds F.C. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 2002, 5:366-371.
30. Graham R., Hell P. On the History of the Minimum Spanning Tree Problem. Ann. Hist. Comput. 1985, 7:43-57.
31. Graser Y., Volovsek M., Arrington J., Schonian G., Presber W., Mitchell T.G., Vilgalys R. Molecular markers reveal that population structure of the human pathogen Candida albicans exhibits both clonality and recombination. Proc. Natl. Acad. Sci. USA 1996, 93:12473-12477.
32. Hube B., Naglik J. Extracellular hydrolases. Candida and Candidiasis 2002, 107-122. ASM Press, Washington, DC. R.A. Calderone (Ed.).
33. Hunter P.R., Gaston M.A. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J. Clin. Microbiol. 1988, 26:2465-2466.
34. Koskinen M.T., Hirvonen H., Landry P.A., Primmer C.R. The benefits of increasing the number of microsatellites utilized in genetic population studies: an empirical perspective. Hereditas 2004, 141:61-67.
35. Kuhner M.K., Felsenstein J. A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol. Biol. Evol. 1994, 11:459-468.
36. Kullberg B.J., Filler S.G. Candidemia. Candida and Candidiasis 2002, 327-340. ASM Press, Wasgington, DC. R.A. Calderone (Ed.).
37. Llewellyn M.S., Miles M.A., Carrasco H.J., Lewis M.D., Yeo M., Vargas J., Torrico F., Diosque P., Valente V., Valente S.A., Gaunt M.W. Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog. 2009, 5:e1000410.
38. Lott T.J., Effat M.M. Evidence for a more recently evolved clade within a Candida albicans North American population. Microbiology 2001, 147:1687-1692.
39. Lunel F.V., Licciardello L., Stefani S., Verbrugh H.A., Melchers W.J., Meis J.F., Scherer S., van Belkum A. Lack of consistent short sequence repeat polymorphisms in genetically homologous colonizing and invasive Candida albicans strains. J. Bacteriol. 1998, 180:3771-3778.
40. Luu L.N., Cowen L.E., Sirjusingh C., Kohn L.M., Anderson J.B. Multilocus genotyping indicates that the ability to invade the bloodstream is widespread among Candida albicans isolates. J. Clin. Microbiol. 2001, 39:1657-1660.
41. MacCallum D.M., Castillo L., Nather K., Munro C.A., Brown A.J., Gow N.A., Odds F.C. Property differences among the four major Candida albicans strain clades. Eukaryot. Cell 2009, 8:373-387.
42. Mathews H.L., Witek-Janusek L. 2002, 179-192. ASM Press, Washington, DC.
43. Michener C.D., Sokal R.R. A quantitative approach to a problem in classification. Evolution 1957, 11:130-162.
44. Naidoo R., Chetty R. The application of microsatellites in molecular pathology. Pathol. Oncol. Res. 1998, 4:310-315.
45. Odds F. Ecology and Epidemiology of Candidiasis 1988, University Park Press, Baltimore.
46. Odds F.C. In Candida albicans, resistance to flucytosine and terbinafine is linked to MAT locus homozygosity and multilocus sequence typing clade 1. FEMS Yeast Res. 2009, 9:1091-1101.
47. Odds F.C. Molecular phylogenetics and epidemiology of Candida albicans. Future Microbiol. 2010, 5:67-79.
48. 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.
49. Orti G., Pearse D.E., Avise J.C. Phylogenetic assessment of length variation at a microsatellite locus. Proc. Natl. Acad. Sci. USA 1997, 94:10745-10749.
50. Piertney S.B., MacColl A.D., Bacon P.J., Dallas J.F. Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers. Mol. Ecol. 1998, 7:1645-1654.
51. Pittet D., Monod M., Suter P.M., Frenk E., Auckenthaler R. Candida colonization and subsequent infections in critically ill surgical patients. Ann. Surg. 1994, 220:751-758.
52. Pujol C., Joly S., Lockhart S.R., Noel S., Tibayrenc M., Soll D.R. Parity among the randomly amplified polymorphic DNA method, multilocus enzyme electrophoresis, and Southern blot hybridization with the moderately repetitive DNA probe Ca3 for fingerprinting Candida albicans. J. Clin. Microbiol. 1997, 35:2348-2358.
53. Pujol C., Pfaller M.A., Soll D.R. Flucytosine resistance is restricted to a single genetic clade of Candida albicans. Antimicrob. Agents Chemother. 2004, 48:262-266.
54. Robles J.C., Koreen L., Park S., Perlin D.S. Multilocus sequence typing is a reliable alternative method to DNA fingerprinting for discriminating among strains of Candida albicans. J. Clin. Microbiol. 2004, 42:2480-2488.
55. Romani L. Immunology of invasive candidiasis. Candida and Candidiasis 2002, 223-241. ASM Press, Washington, DC. R.A. Calderone (Ed.).
56. Rosenblum B.B., Oaks F., Menchen S., Johnson B. Improved single-strand DNA sizing accuracy in capillary electrophoresis. Nucleic Acids Res. 1997, 25:3925-3929.
57. Ross K.G., Shoemaker D.D., Krieger M.J., DeHeer C.J., Keller L. Assessing genetic structure with multiple classes of molecular markers: a case study involving the introduced fire ant Solenopsis invicta. Mol. Biol. Evol. 1999, 16:525-543.
58. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
59. Sampaio P., Gusmao L., Alves C., Pina-Vaz C., Amorim A., Pais C. Highly polymorphic microsatellite for identification of Candida albicans strains. J. Clin. Microbiol. 2003, 41:552-557.
60. Sampaio P., Gusmao L., Correia A., Alves C., Rodrigues A.G., Pina-Vaz C., Amorim A., Pais C. New microsatellite multiplex PCR for Candida albicans strain typing reveals microevolutionary changes. J. Clin. Microbiol. 2005, 43:3869-3876.
61. Schmid J., Herd S., Hunter P.R., Cannon R.D., Yasin M.S., Samad S., Carr M., Parr D., McKinney W., Schousboe M., Harris B., Ikram R., Harris M., Restrepo A., Hoyos G., Singh K.P. Evidence for a general-purpose genotype in Candida albicans, highly prevalent in multiple geographical regions, patient types and types of infection. Microbiology 1999, 145:2405-2413.
62. Schouls L.M., van der Heide H.G., Vauterin L., Vauterin P., Mooi F.R. Multiple-locus variable-number tandem repeat analysis of Dutch Bordetella pertussis strains reveals rapid genetic changes with clonal expansion during the late 1990s. J. Bacteriol. 2004, 186:5496-5505.
63. Soll D.R. The ins and outs of DNA fingerprinting the infectious fungi. Clin. Microbiol. Rev. 2000, 13:332-370.
64. Soll D.R. Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop. 2002, 81:101-110.
65. Soll D.R., Pujol C. Candida albicans clades. FEMS Immunol. Med. Microbiol. 2003, 39:1-7.
66. Spellberg B., Edwards J.E. The pathophysiology and treatment of Candida sepsis. Curr. Infect. Dis. Rep. 2002, 4:387-399.
67. Sundstrom P. Adhesion in Candida spp. Cell. Microbiol. 2002, 4:461-469.
68. 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.
69. Taylor J.W., Geiser D.M., Burt A., Koufopanou V. The evolutionary biology and population genetics underlying fungal strain typing. Clin. Microbiol. Rev. 1999, 12:126-146.
70. Wenz H., Robertson J.M., Menchen S., Oaks F., Demorest D.M., Scheibler D., Rosenblum B.B., Wike C., Gilbert D.A., Efcavitch J.W. High-precision genotyping by denaturing capillary electrophoresis. Genome Res. 1998, 8:69-80.
71. Xu J., Mitchell T.G. Population genetic analyses of Candida. Candida and Candidiasis 2002, ASM Press, Washington, DC. R.A. Calderone (Ed.).
72. Yue G.H., Kovacs B., Orban L. A new problem with cross-species amplification of microsatellites: generation of non-homologous products. Dongwuxue Yanjiu 2010, 31:131-140.