Genetic diversity of the Cryptococcus species complex suggests that Cryptococcus gattii deserves to have varieties

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Ngamskulrungroj, Popchai ^a,b,c   Gilgado, Felix ^a,b   Faganello, Josiane ^d   Litvintseva, Anastasia P ^e   Leal, Ana Luisa ^d   Tsui, Kin Ming ^a,b   Mitchell, Thomas G ^c   Vainstein, Marilene Henning ^d   Meyer, Wieland ^a,b  

^a WESTMEAD HOSPITAL   (Australia)

^b University of Sydney   (Australia)

^c MAHIDOL UNIVERSITY   (Thailand)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; INSULINASE; OROTIDINE 5' PHOSPHATE DECARBOXYLASE; PHOSPHOLIPASE; PHOSPHOLIPASE B1; UNCLASSIFIED DRUG;

ARTICLE; BASIDIOMYCETES; CLADISTICS; CONTROLLED STUDY; CRYPTOCOCCUS; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; FUNGAL GENETICS; FUNGAL STRAIN; GENE LOCUS; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; HAPLOIDY; MOLECULAR CLOCK; MOLECULAR TYPING; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARSIMONY ANALYSIS; PHYLOGENY; SEQUENCE ANALYSIS; STRAIN DIFFERENCE; TAXONOMY; UNINDEXED SEQUENCE; ANIMAL; CELL LINEAGE; DNA SEQUENCE; FUNGAL GENE; GENETICS; HUMAN; METHODOLOGY; MICROBIOLOGICAL EXAMINATION; MOLECULAR GENETICS; PHYSIOLOGY; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE;

CRYPTOCOCCUS GATTII; FILOBASIDIELLA NEOFORMANS; MAMMALIA;

ANIMALS; BASE SEQUENCE; CELL LINEAGE; CRYPTOCOCCUS; GENES, MATING TYPE, FUNGAL; GENETIC VARIATION; HAPLOIDY; HUMANS; MOLECULAR SEQUENCE DATA; MYCOLOGICAL TYPING TECHNIQUES; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY;

EID: 67649222249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005862     Document Type: Article

References (83)

1. Casadevall A, Perfect JR (1998) Cryptococcus neoformans. Washington, DC: ASM press.
2. Kwon-Chung KJ, Bennett JE (1984) Epidemiologic differences between the two varieties of Cryptococcus neoformans. Am J Epidemiol 120: 123-130.
3. Franzot SP, Fries BC, Cleare W, Casadevall A (1998) Genetic relationship between Cryptococcus neoformans var. neoformans strains of serotypes A and D. J Clin Microbiol 36: 2200-2204.
4. Kwon-Chung KJ, Boekhout T, Fell JW, Diaz M (2002) (1557) Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. basillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae). Taxon 51: 804-806.
5. Sorrell TC (2001) Cryptococcus neoformans variety gattii. Med Mycol 39: 155-168.
6. Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, et al. (2004) A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci U S A 101: 17258-17263.
7. Meyer W, Marszewska K, Amirmostofian M, Igreja RP, Hardtke C, et al. (1999) Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA-a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 20: 1790-1799.
8. Boekhout T, Theelen B, Diaz M, Fell JW, Hop WC, et al. (2001) Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans. Microbiology 147: 891-907.
9. Meyer W, Castaneda A, Jackson S, Huynh M, Castaneda E (2003) Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg Infect Dis 9: 189-195.
10. Latouche GN, Huynh M, Sorrell TC, Meyer W (2003) PCR-restriction fragment length polymorphism analysis of the phospholipase B (PLB1) gene for subtyping of Cryptococcus neoformans isolates. Appl Environ Microbiol 69: 2080-2086.
11. Xu J, Vilgalys R, Mitchell TG (2000) Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neoformans. Mol Ecol 9: 1471-1481.
12. Diaz MR, Boekhout T, Kiesling T, Fell JW (2005) Comparative analysis of the intergenic spacer regions and population structure of the species complex of the pathogenic yeast Cryptococcus neoformans. FEMS Yeast Res 5: 1129-1140.
13. Butler MI, Poulter RT (2005) The PRP8 inteins in Cryptococcus are a source of phylogenetic and epidemiological information. Fungal Genet Biol 42: 452-463.
14. Bovers M, Hagen F, Kuramae EE, Boekhout T (2008) Six monophyletic lineages identified within Cryptococcus neoformans and Cryptococcus gattii by multi-locus sequence typing. Fungal Genet Biol 45: 400-421.
15. Litvintseva AP, Thakur R, Vilgalys R, Mitchell TG (2006) Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. grubii (serotype A), including a unique population in Botswana. Genetics 172: 2223-2238.
16. Bovers M, Hagen F, Kuramae EE, Diaz MR, Spanjaard L, et al. (2006) Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res 6: 599-607.
17. Cox GM, Rude TH, Dykstra CC, Perfect JR (1995) The actin gene from Cryptococcus neoformans: structure and phylogenetic analysis. J Med Vet Mycol 33: 261-266.
18. Cox GM, McDade HC, Chen SC, Tucker SC, Gottfredsson M, et al. (2001) Extracellular phospholipase activity is a virulence factor for Cryptococcus neoformans. Mol Microbiol 39: 166-175.
19. Faganello J, Dutra V, Schrank A, Meyer W, Schrank IS, et al. (2008) Identification of genomic differences between Cryptococcus neoformans and Cryptococcus gattii by Representational Difference Analysis (RDA). Med Mycol. pp 1-8.
20. Duckworth WC, Bennett RG, Hamel FG (1998) Insulin degradation: progress and potential. Endocr Rev 19: 608-624.
21. Chesneau V, Rosner MR (2000) Functional human insulin-degrading enzyme can be expressed in bacteria. Protein Expr Purif 19: 91-98.
22. Garcia JV, Gehm BD, Rosner MR (1989) An evolutionarily conserved enzyme degrades transforming growth factor-alpha as well as insulin. J Cell Biol 109: 1301-1307.
23. Authier F, Bergeron JJ, Ou WJ, Rachubinski RA, Posner BI, et al. (1995) Degradation of the cleaved leader peptide of thiolase by a peroxisomal proteinase. Proc Natl Acad Sci U S A 92: 3859-3863.
24. Igreja RP, Lazera Mdos S, Wanke B, Galhardo MC, Kidd SE, et al. (2004) Molecular epidemiology of Cryptococcus neoformans isolates from AIDS patients of the Brazilian city, Rio de Janeiro. Med Mycol 42: 229-238.
25. Katsu M, Kidd S, Ando A, Moretti-Branchini ML, Mikami Y, et al. (2004) The internal transcribed spacers and 5.8S rRNA gene show extensive diversity among isolates of the Cryptococcus neoformans species complex. FEMS Yeast Res 4: 377-388.
26. Escandon P, Sanchez A, Martinez M, Meyer W, Castaneda E (2006) Molecular epidemiology of clinical and environmental isolates of the Cryptococcus neoformans species complex reveals a high genetic diversity and the presence of the molecular type VGII mating type a in Colombia. FEMS Yeast Res 6: 625-635.
27. Wickes BL, Moore TD, Kwon-Chung KJ (1994) Comparison of the electrophoretic karyotypes and chromosomal location of ten genes in the two varieties of Cryptococcus neoformans. Microbiology 140 (Pt 3): 543-550.
28. Fraser JA, Subaran RL, Nichols CB, Heitman J (2003) Recapitulation of the sexual cycle of the primary fungal pathogen Cryptococcus neoformans var. gattii: implications for an outbreak on Vancouver Island, Canada. Eukaryot Cell 2: 1036-1045.
29. Varma A, Kwon-Chung KJ (1998) Construction of stable episomes in Cryptococcus neoformans. Curr Genet 34: 60-66.
30. Cunningham CW (1997) Can three incongruence tests predict when data should be combined? Mol Biol Evol 14: 733-740.
31. Litvintseva AP, Marra RE, Nielsen K, Heitman J, Vilgalys R, et al. (2003) Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukaryot Cell 2: 1162-1168.
32. Trilles L, Lazera M, Wanke B, Theelen B, Boekhout T (2003) Genetic characterization of environmental isolates of the Cryptococcus neoformans species complex from Brazil. Med Mycol 41: 383-390.
33. Kwon-Chung KJ, Bennett JE (1978) Distribution of alpha and alpha mating types of Cryptococcus neoformans among natural and clinical isolates. Am J Epidemiol 108: 337-340.
34. McClelland CM, Chang YC, Varma A, Kwon-Chung KJ (2004) Uniqueness of the mating system in Cryptococcus neoformans. Trends Microbiol 12: 208-212.
35. Campbell LT, Currie BJ, Krockenberger M, Malik R, Meyer W, et al. (2005) Clonality and recombination in genetically differentiated subgroups of Cryptococcus gattii. Eukaryot Cell 4: 1403-1409.
36. Halliday CL, Carter DA (2003) Clonal reproduction and limited dispersal in an environmental population of Cryptococcus neoformans var gattii isolates from Australia. J Clin Microbiol 41: 703-711.
37. Sriburee P, Khayhan S, Khamwan C, Panjaisee S, Tharavichitkul P (2004) Serotype and PCR-fingerprints of clinical and environmental isolates of Cryptococcus neoformans in Chiang Mai, Thailand. Mycopathologia 158: 25-31.
38. Taylor J, Jacobson D, Fisher M (1999) The evolution of asexual fungi: Reproduction, Speciation and Classification. Annu Rev Phytopathol 37: 197-246.
39. Pringle A, Baker DM, Platt JL, Wares JP, Latge JP, et al. (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59: 1886-1899.
40. Maynard-Smith JM, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria?
41. Boekhout T, van Belkum A (1997) Variability of karyotypes and RAPD types in genetically related strains of Cryptococcus neoformans. Curr Genet 32: 203-208.
42. Xu J, Mitchell TG (2003) Comparative gene genealogical analyses of strains of serotype AD identify recombination in populations of serotypes A and D in the human pathogenic yeast Cryptococcus neoformans. Microbiology 149: 2147-2154.
43. Kidd SE, Guo H, Bartlett KH, Xu J, Kronstad JW (2005) Comparative gene genealogies indicate that two clonal lineages of Cryptococcus gattii in British Columbia resemble strains from other geographical areas. Eukaryot Cell 4: 1629-1638.
44. Campbell LT, Fraser JA, Nichols CB, Dietrich FS, Carter D, et al. (2005) Clinical and environmental isolates of Cryptococcus gattii from Australia that retain sexual fecundity. Eukaryot Cell 4: 1410-1419.
45. Saul N, Krockenberger M, Carter D (2008) Evidence of recombination in mixed-mating-type and alpha-only populations of Cryptococcus gattii sourced from single eucalyptus tree hollows. Eukaryot Cell 7: 727-734, 69.
46. Bui T, Lin X, Malik R, Heitman J, Carter D (2008) Isolates of Cryptococcus neoformans from infected animals reveal genetic exchange in unisexual, {alpha} mating type populations. Eukaryot Cell 7: 1771-1780.
47. Campbell LT, Carter DA (2006) Looking for sex in the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii. FEMS Yeast Res 6: 588-598.
48. Sharpton TJ, Neafsey DE, Galagan JE, Taylor JW (2008) Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 9: R24.
49. Litvintseva AP, Lin X, Templeton I, Heitman J, Mitchell TG (2007) Many globally isolated AD hybrid strains of Cryptococcus neoformans originated in Africa. PLoS Pathog 3: e114.
50. Escandon P, Ngamskulrungroj P, Meyer W, Castaneda E (2007) In vitro mating of Colombian isolates of the Cryptococcus neoformans species complex. Biomedica 27: 308-314.
51. Ngamskulrungroj P, Sorrell TC, Chindamporn A, Chaiprasert A, Poonwan N, et al. (2008) Association between fertility and molecular sub-type of global isolates of Cryptococcus gattii molecular type VGII. Med Mycol 46: 665-673.
52. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, et al. (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31: 21-32.
53. Mayden RL (1997) A hierarchy of species concepts: the denouncement in the saga of the species problem. In: Claridge MF, Dawah HA, Wilson MR, eds. Species: the units of biodiversity. London: Chapman and Hall. pp 381-424.
54. Cogliati M, Esposto MC, Tortorano AM, Viviani MA (2006) Cryptococcus neoformans population includes hybrid strains homozygous at mating-type locus. FEMS Yeast Res 6: 608-613.
55. Lengeler KB, Cox GM, Heitman J (2001) Serotype AD strains of Cryptococcus neoformans are diploid or aneuploid and are heterozygous at the mating-type locus. Infect Immun 69: 115-122.
56. Mayr E (1942) Systematics and the origin of species: from the viewpoint of a zoologist. New York: Columbia University Press. 334 p.
57. Halliday CL, Bui T, Krockenberger M, Malik R, Ellis DH, et al. (1999) Presence of alpha and a mating types in environmental and clinical collections of Cryptococcus neoformans var. gattii strains from Australia. J Clin Microbiol 37: 2920-2926.
58. Kwon-Chung KJ, Bennett JE, Rhodes JC (1982) Taxonomic studies on Filobasidiella species and their anamorphs. Antonie Van Leeuwenhoek 48: 25-38.
59. Loftus BJ, Fung E, Roncaglia P, Rowley D, Amedeo P, et al. (2005) The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans. Science 307: 1321-1324.
60. Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
61. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.
62. Kidd S (2003) Molecular Epidemiology and Characterisation of Genetic Structure to Assess Speciation within the Cryptococcus neoformans Complex. Westmead: The University of Sydney. 429 p.
63. Swofford D (2001) PAUP*. Phylogenetic using parsimony (* and other methods). 4 ed. Sunderland, MA: Sinauer.
64. Huelsenbeck J, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Oxford. pp 754-755.
65. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.
66. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
67. Farris JS, Kallersjo M, Kluge AG, Bult C (1995) Testing significance of incongruence. Cladistics 10: 315-319.
68. Huelsenbeck JP, Bull JJ, Cunningham CW (1996) Combining data in phylogenetic analysis. Trends Ecol Evol 11: 152-158.
69. Taylor JW, Geiser DM, Burt A, Koufopanou V (1999) The evolutionary biology and population genetics underlying fungal strain typing. Clin Microbiol Rev 12(1): 126-146.
70. Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1: 101-102.
71. Estabrook GF, Landrum L (1975) A simple test for the possible simultaneous evolutionary divergence of two amino acid positions. Taxon 24: 609-613.
72. Stephens JC, Nei M (1985) Phylogenetic analysis of polymorphic DNA sequences at the Adh locus in Drosophila melanogaster and its sibling species. J Mol Evol 22: 289-300.
73. Li WH, Tanimura M, Sharp PM (1987) An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J Mol Evol 25: 330-342.
74. Espinel-Ingroff A, Kish CW Jr, Kerkering TM, Fromtling RA, Bartizal K, et al. (1992) Collaborative comparison of broth macrodilution and microdilution antifungal susceptibility tests. J Clin Microbiol 30: 3138-3145.
75. Perfect JR, Ketabchi N, Cox GM, Ingram CW, Beiser CL (1993) Karyotyping of Cryptococcus neoformans as an epidemiological tool. J Clin Microbiol 31: 3305-3309.
76. Meyer W, Lieckfeldt E, Kuhls K, Freedman EZ, Borner T, et al. (1993) DNA-and PCR-fingerprinting in fungi. Exs 67: 311-320.
77. Kwon-Chung KJ, Edman JC, Wickes BL (1992) Genetic association of mating types and virulence in Cryptococcus neoformans. Infect Immun 60: 602-605.
78. Chen S, Sorrell T, Nimmo G, Speed B, Currie B, et al. (2000) Epidemiology and host- and variety-dependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Australasian Cryptococcal Study Group. Clin Infect Dis 31: 499-508.
79. Sukroongreung S, Nilakul C, Ruangsomboon O, Chuakul W, Eampokalap B (1996) Serotypes of Cryptococcus neoformans isolated from patients prior to and during the AIDS era in Thailand. Mycopathologia 135: 75-78.
80. Fraser JA, Giles SS, Wenink EC, Geunes-Boyer SG, Wright JR, et al. (2005) Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437: 1360-1364.
81. Velegraki A, Kiosses VG, Pitsouni H, Toukas D, Daniilidis VD, et al. (2001) First report of Cryptococcus neoformans var. gattii serotype B from Greece. Med Mycol 39: 419-422.
82. Samson RA, Stalpers JA, Weijman AC (1983) On the taxonomy of the entomogenous fungus Filobasidiella arachnophila. Antonie Van Leeuwenhoek 49: 447-456.
83. Kooiman P (1963) The Chemical Structure of the Extracellular "Starch" Produced by Cryptococcus Albidus and C. Laurentii Var. Flavescens. Antonie Van Leeuwenhoek 29: 169-176.