Molecular Typing of the Cryptococcus neoformans/Cryptococcus gattii Species Complex
Wieland Meyer
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorFelix Gilgado
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorPopchai Ngamskulrungroj
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorLuciana Trilles
Mycology Laboratory, Instituto de Pesquisa Clínica Evandro Chagas (IPEC), Fundação Oswaldo Cruz (FIOCRUZ), 21040-900 Rio de Janeiro, Brazil
Search for more papers by this authorFerry Hagen
CBS-KNAW Fungal Diversity Centre, NL-3584CT Utrecht, The Netherlands
Search for more papers by this authorElizabeth Castañeda
Emerita Investigator, Instituto Nacional de Salud, Bogotá, Colombia
Search for more papers by this authorTeun Boekhout
CBS-KNAW Fungal Diversity Centre, NL-3584CT Utrecht, The Netherlands
Search for more papers by this authorWieland Meyer
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorFelix Gilgado
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorPopchai Ngamskulrungroj
Molecular Mycology Research Laboratory, Centre for Infectious Diseases and Microbiology, University of Sydney, Sydney Medical School - Westmead at Westmead Hospital, Westmead Millennium Institute, Westmead, NSW, 2145 Australia
Search for more papers by this authorLuciana Trilles
Mycology Laboratory, Instituto de Pesquisa Clínica Evandro Chagas (IPEC), Fundação Oswaldo Cruz (FIOCRUZ), 21040-900 Rio de Janeiro, Brazil
Search for more papers by this authorFerry Hagen
CBS-KNAW Fungal Diversity Centre, NL-3584CT Utrecht, The Netherlands
Search for more papers by this authorElizabeth Castañeda
Emerita Investigator, Instituto Nacional de Salud, Bogotá, Colombia
Search for more papers by this authorTeun Boekhout
CBS-KNAW Fungal Diversity Centre, NL-3584CT Utrecht, The Netherlands
Search for more papers by this authorJoseph Heitman
Duke University Medical Center, Durham, NC, 27710
Search for more papers by this authorThomas R. Kozel
University of Nevada School of Medicine, Reno, NV, 89557-0320
Search for more papers by this authorKyung J. Kwon-Chung
National Institute of Allergy and Infectious Diseases, Bethesda, MD, 20892
Search for more papers by this authorJohn R. Perfect
Duke University Medical Center, Durham, NC, 27710
Search for more papers by this authorArturo Casadevall
Albert Einstein College of Medicine, Bronx, NY, 10461
Search for more papers by this authorSummary
A large number of molecular typing techniques have been applied over the years to discriminate between individual isolates that had been indistinguishable using conventional techniques and to obtain further insights into the epidemiology and population structure of this species complex. This chapter aims to summarize the diverse typing techniques applied to the Cryptococcus neoformans/C. gattii species complex, to correlate the obtained results, and to describe the global distribution of the major genotypes. The enzymes malate dehydrogenase, alcohol dehydrogenase, phosphoglyceromutase, and glutamate dehydrogenase could separate C. gattii from C. neoformans. Electrophoretic karyotyping was for the first time applied to the C. neoformans/C. gattii species complex to study the genetic diversity between seven cryptococcal strains representing all four serotypes. PCR fingerprinting using the primer (GACA)4 was applied to 110 cryptococcal isolates obtained mainly from Germany and Africa as well as additional globally collected reference strains. The restriction fragment length polymorphism (RFLP) patterns result from the presence of a restriction enzyme cleavage site at one place in the genome in one individual and the absence of that specific site in another individual. Intergenic spacer (IGS) sequence analysis is a powerful tool to delineate the two varieties of C. neoformans and separate the four major molecular types of C. gattii.
References
- Abegg, M. A., F. L. Cella, J. Faganello, P. Valente, A. Schrank, and M. H. Vainstein. 2006. Cryptococcus neoformans and Cryptococcus gattii isolated from the excreta of Psittaciformes in a southern Brazilian zoological garden. My-copathologia 161: 83–91.
- Almeida, A. M. F., M. T. Matsumoto, L. C. Baeza, R. B. de Oliveira e Silva, A. A. P. Kleiner, M. de Souza Carv-alho Melhem, M. J. S. M. Giannini, and the Laboratory Group on Cryptococcosis. 2006. Molecular typing and an-tifungal susceptibility of clinical sequential isolates of Cryp-tococcus neoformans from Sao Paulo State, Brazil. FEMS Yeast Res. 7: 152–164.
- Barreto de Oliveira, M. T., T. Boekhout, B. Theelen, F. Hagen, F. A. Baroni, M. S. Lazera, K. B. Lengeler, J. Heitman, I. N. Rivera, and C. R. Paula. 2004. Cryptococcus neoformans shows a remarkable genotypic diversity in Brazil. J. Clin. Microbiol. 42: 1356–1359.
- Bertout, S., F. Renaud, D. Swinne, M. Mallie, and J. M. Bastide. 1999. Genetic multilocus studies of different strains of Cryptococcus neoformans: taxonomy and genetic structure. J. Clin. Microbiol. 37: 715–720.
- Boekhout, T., M. Renting, W. A. Scheffers, and R. Bos-boom. 1993. The use of karyotyping in the systematics of yeasts. Antonie Van Leeuwenhoek 63: 157–163.
- Boekhout, T., B. Theelen, M. Diaz, J. W. Fell, W. C. Hop, E. C. Abeln, F. Dromer, and W. Meyer. 2001. Hybrid genotypes in the pathogenic yeast Cryptococcus neoformans . Microbiology 147: 891–907.
- Boekhout, T., and A. van Belkum. 1997. Variability of karyotypes and RAPD types in genetically related strains of Cryptococcus neoformans . Curr. Genet. 32: 203–208.
- Boekhout, T., A. van Belkum, A. C. Leenders, H. A. Verbrugh, P. Mukamurangwa, D. Swinne, and W. A. Scheffers. 1997. Molecular typing of Cryptococcus neoformans: taxonomic and epidemiological aspects. Int. J. Syst. Bacteriol. 47: 432–442.
- Bolton, L. A., R. G. Lobetti, D. N. Evezard, J. A. Picard, J. W. Nesbit, J. van Heerden, and R. E. Burroughs. 1990. Cryptococcosis in captive cheetah (Acinonyx jubatus): two cases. J. S. Afr. Vet. Assoc. 70: 35–39.
- Bovers, M., F. Hagen, and T. Boekhout. 2008. Diversity of the Cryptococcus neoformans- Cryptococcus gattii species complex. Rev. Iberoam. Micol. 25: S4–S12.
- Bovers, M., F. Hagen, E. E. Kuramae, and T. Boekhout. 2008. Six monophyletic lineages identified within Crypto-coccus neoformans and Cryptococcus gattii by multi-locus sequence typing. Fungal Genet. Biol. 45: 400–421.
- Bovers, M., F. Hagen, E. E. Kuramae, and T. Boekhout. 2009. Promiscuous mitochondria in Cryptococcus gattii . FEMS Yeast Res. 9: 489–503.
- Bovers, M., F. Hagen, E. E. Kuramae, M. R. Diaz, L. Spanjaard, F. Dromer, H. L. Hoogveld, and T. Boek-hout. 2006. Unique hybrids between the fungal pathogens Cryptococcus neoformans and Cryptococcus gattii . FEMS Yeast Res. 6: 599–607.
- Bovers, M., F. Hagen, E. E. Kuramae, H. L. Hoogveld, F. Dromer, G. St-Germain, and T. Boekhout. 2008c. AIDS patient death caused by novel Cryptococcus neofor-mans x C. gattii hybrid. Emerg. Infect. D is. 14: 1105–1108.
- Brandt, M. E., S. L. Bragg, and R. W. Pinner. 1993. Mul-tilocus enzyme typing of Cryptococcus neoformans . J. Clin. Microbiol. 31: 2819–2823.
- Brandt, M. E., M. A. Pfaller, R. A. Hajjeh, E. A. Graviss, J. Rees, E. D. Spitzer, R. W. Pinner, L. W. Mayer, and the Cryptococcal Disease Active Surveillance Group. 1996. Molecular subtypes and antifungal susceptibilities of serial Cryptococcus neoformans isolates in human immunodeficiency virus-associated cryptococcosis. J. Infect. Dis. 174: 812–820.
- Byrnes, E. J., 3rd, R. J. Bildfell, S. A. Frank, T. G. Mitchell, K. A. Marr, and J. Heitman. 2009. Molecular evidence that the range of the Vancouver Island outbreak of Cryptococcus gattii infection has expanded into the Pacific Northwest in the United States. J. Infect. Dis. 199: 1081–1086.
- Calvo, B. M., A. L. Colombo, O. Fischman, A. Santiago, L. Thompson, M. Lazera, F. Telles, K. Fukushima, K. Nishimura, R. Tanaka, M. Myiajy, and M. L. Moretti-Branchini. 2001. Antifungal susceptibilities, varieties, and electrophoretic karyotypes of clinical isolates of Cryptococ-cus neoformans from Brazil, Chile, and Venezuela. J. Clin. Microbiol. 39: 2348–2350.
- Campbell, L. T., B. J. Currie, M. Krockenberger, R. Malik, W. Meyer, J. Heitman, and D. Carter. 2005. Clonality and recombination in genetically differentiated subgroups of Cryptococcus gattii . Eukaryot. Cell 4: 1403–1409.
- Casali, A. K., L. Goulart, L. K. Silva, A. M. Ribeiro, A. A. Amaral, S. H. Alves, A. Schrank, W. Meyer, and M. H. Vainstein. 2003. Molecular typing of clinical and environmental Cryptococcus neoformans isolates in the Brazilian State Rio Grande do Sul. FEMS Yeast Res. 3: 405–415.
- Castañón-Olivares, L. R., K. Martínez-Martínez, R. M. Bermúdez-Cruz, M. A. Martínez-Rivera, R. A. Arreguín-Espinosa, R. A. López-Martínez, W. Meyer, and G. M. Ruiz-Palacios y Santos. 2009. Genotyping of Mexican Cryptococcus neoformans and C. gattii isolates by PCR-fingerprinting. Med. Mycol. 47: 713–721.
- Chen, J. A. Varma, M. R. Diaz, A. P. Litvintseva, K. K. Wollenberg, and K. J. Kwon-Chung. 2008. Cryptococcus neoformans strains and infection in apparently immunocom-petent patients, China. Emerg. Infect. Dis. 14: 755–762.
- Chen, S., T. Sorrell, G. Nimmo, B. Speed, B. Currie, D. Ellis, D. Marriott, T. Pfeiffer, D. Parr, K. Byth, and the Australasian Cryptococcal Study Group. 2000. Epidemiology and host- and variety-dependent characteristics of infection due to Cryptococcus neoformans in Australia and New Zealand. Clin. Infect. Dis. 31: 449–508.
- Chen, S. C. A., A. Brownlee, T. Sorrell, P. Ruma, D. H. Ellis, T. Pfeiffer, B. R. Speed, and G. Nimmo. 1996. Identification by random amplification of polymorphic DNA (RAPD) of a common molecular type of C. neofor-mans var. neoformans in patients with AIDS. J. Infect. Dis. 173: 754–758.
- Chen, S. C. A., B. J. Currie, H. M. Campbell, D. A. Fisher, T. J. Pfeiffer, D. H. Ellis, and T. C. Sorrell. 1997. Cryptococcus neoformans var. gattii infection in northern Australia: existence of an environmental source other than known host eucalypts. Trans. R. Soc. Trop. Med. Hyg. 91: 547–550.
- Chen, Y., F. Che, F. Wei, N. Xu, M. Yang, and J. Chen. 2008. Cryptococcosis in China from 1985 to 2007. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-01–01.
- Cogliati, M., M. Allaria, A. M. Tortorano, and M. A. Viviani. 2000. Genotyping Cryptococcus neoformans var. neoformans with specific primers designed from PCR-fingerprinting bands sequenced using a modified PCR-based strategy. Med. Mycol. 38: 97–103.
- Cogliati, M., N. Chandrashekar, A. Prigitano, M. C. Esposto, B. Petrini, A. Chandramuki, and M. A. Vivi-ani. 2008. Clinical isolates from an Indian hospital: an unexpected detection of a serotype C Cryptococcus gattii population. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-05–04.
- Cogliati, M., M. C. Esposto, A. M. Tortorano, and M. A. Viviani. 2006. Cryptococcus neoformans population includes hybrid strains homozygous at mating-type locus. FEMS Yeast Res. 6: 608–613.
- Cogliati, M., M. C. Esposto, G. Liberi, A. M. Tortorano, and M. A. Viviani. 2007. Cryptococcus neoformans typing by PCR fingerprinting using (GACA)4 primer: a new light on the basis of Cryptococcus neoformans genome project data. J. Clin. Microbiol. 45: 3427–3430.
- Crampin, A. C., R. C. Matthews, D. Hall, and E. G. V. Evans. 1993. PCR fingerprinting of C. neoformans by random amplification of polymorphic DNA. J. Med. Vet. Mycol. 31: 463–465.
- Currie, B. P., L. F. Freundlich, and A. Casadevall. 1994. Restriction fragment length polymorphism analysis of Cryptococcus neoformans isolates from environmental (pigeon excreta) and clinical sources in New York City. J. Clin. Microbiol. 32: 1188–1192.
- Diaz, M. R., T. Boekhout, T. Kiesling, and J. W. Fell. 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.
- Diaz, M. R., T. Boekhout, B. Theelen, and J. W. Fell. 2000. Molecular sequence analysis of the intergenic spacer (IGS) associated with rDNA of the two varieties of the pathogenic yeast, Cryptococcus neoformans. Syst. Appl. Microbiol. 23: 535–545.
- Diaz, M. R., and J. W. Fell. 2000. Molecular analysis of the IGS & ITS regions of rDNA of the psychrophilic yeasts in the genus Mrakia . Antonie van Leeuwenhoek 77: 7–12.
- Dromer, F., A. Varma, O. Ronin, S. Mathoulin, and B. Dupont. 1994. Molecular typing of Cryptococcus neo-formans serotype D clinical isolates. J. Clin. Microbiol. 32: 2364–2371.
- D'Souza, C. A., F. Hagen, T. Boekhout, G. M. Cox, and J. Heitman. 2004. Investigation of the basis of virulence in serotype A strains of Cryptococcus neoformans from apparently immunocompetent individuals. Curr. Genet. 46: 92–102.
- Ellis, D., D. Marriott, R. A. Hajjeh, D. Warnock, W. Meyer, and R. Barton. 2000. Epidemiology: surveillance of fungal infections. Med. Mycol. 38 (Suppl. 1): 173–182.
-
Epplen, J., and T. Lubjuhn. 1999. DNA Profiling and DNA Fingerprinting. Birkhauser, Heidelberg, Germany.
10.1007/978-3-0348-7582-0 Google Scholar
- Escandón, P., A. Sánchez, M. Martínez, W. Meyer, and E. Castañeda. 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.
- Evans, E. E. 1950. The antigenic composition of Crypto-coccus neoformans. I. A serologic classification by means of the capsular and agglutination reactions. J. Immunol. 64: 423–430.
- Fan, M., B. P. Currie, R. R. Gutell, M. A. Ragan, and A. Casadevall. 1994. The 16S-like, 5.8S and 23S-like rRNAs of the two varieties of Cryptococcus neoformans: sequence, secondary structure, phylogenetic analysis and restriction fragment polymorphisms. J. Med. Vet. Mycol. 32: 163–180.
- Feng, X., Z. Yao, D. Ren, and W. Liao. 2008. Simultaneous identification of molecular and mating types within the Cryptococcus species complex by PCR-RFLP analysis. J. Med. Microbiol. 57: 1481–1490.
- Feng, X., Z. Yao, D. Ren, W. Liao, and J. Wu. 2008. Genotyping and mating type analyses of Cryptococcus neo-formans and Cryptococcus gattii isolates from China that mainly originated from non-HIV-infected patients. FEMS Yeast Res. 8: 930–938.
- Fraser, J. A., S. S. Giles, E. C. Wenink, S. G. Geunes-Boyer, J. R. Wright, S. Diezmann, A. Allen, J. E. Sta-jich, F. S. Dietrich, J. R. Perfect, and J. Heitman. 2005. Same-sex mating and the origin of the Vancouver Island Cryptococcus gattii outbreak. Nature 437: 1360–1364.
- Franzot, S. P., J. S. Hamdan, B. P. Currie, and A. Casa-devall. 1997. Molecular epidemiology of Cryptococcus neo-formans in Brazil and the United States: evidence for both local genetic differences and a global clonal population structure. J. Clin. Microbiol. 35: 2243–2251.
- Franzot, S. P., I. F. Salkin, and A. Casadevall. 1999. Cryptococcus neoformans var. grubii: separate varietal status for Cryptococcus neoformans serotype A isolates. J. Clin. Microbiol. 37: 838–840.
- Fries, B. C., F. Chen, B. P. Currie, A. Casadevall. 1996. Karyotype instability in Cryptococcus neoformans infection. J. Clin. Microbiol. 34: 1531–1534.
- Garcia-Hermoso, D., F. Dromer, S. Mathoulin-Pelissier, and G. Janbon. 2001. Are two Cryptococcus neoformans strains epidemiologically linked? J. Clin. Microbiol. 39: 1402–1406.
- Garcia-Hermoso, D., S. Mathoulin-Pelissier, B. Coup-rie, O. Ronin, B. Dupont, and F. Dromer. 1997. DNA typing suggests pigeon droppings as a source of pathogenic Cryptococcus neoformans serotype D. J. Clin. Microbiol. 35: 2683–2685.
- Gatti, F., and R. Eeckels. 1970. An atypical strain of Cryptococcus neoformans (Sanfelice) Vuillemin. Part I. Description of the diseases and of the strain. Ann. Soc. Belg. Med. Trop. 50: 689–694.
- Georgi, A., M. Schneemann, K. Tintelnot, R. C. Calligaris-Maibach, S. Meyer, R. Weber, and P. P. Bosshard. 2009. Cryptococcus gattii meningoencephalitis in an immunocompetent person 13 months after exposure. Infection 37: 370–373.
- Gil-Lamaignere, C, E. Roilides, J. Hacker, and F. M. Muller. 2003. Molecular typing for fungi: a critical review of the possibilities and limitations of currently and future methods. Clin. Microbiol. Infect. 9: 172–185.
- Halliday, C. L., T. Bui, M. Krockenberger, R. Malik, D. H. Ellis, and D. A. Carter. 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.
- Halliday, C. L., and D. A. Carter. 2003. Clonal reproduction and limited dispersal in an environmental population of Cryptococcus neoformans var. gattii isolates from Australia. J. Clin. Microbiol. 41: 703–711.
- Hanafy, A., S. Kaocharoen, A. Jover-Botella, M. Katsu, S. Iida, T. Kogure, T. Gonoi, Y. Mikami, and W. Meyer. 2008. Multilocus microsatellite typing for C. neoformans var. grubii . Med. Mycol. 46: 685–696.
- Haynes, K. A., D. J. Sullivan, D. C. Coleman, J. C. K. Clarke, R. Emilianus, C. Atkinson, and K. J. Cann. 1995. Involvement of multiple Cryptococcus neoformans strains in a single episode of cryptococcosis and reinfection with novel strains in recurrent infection demonstrated by random amplification of polymorphic DNA and DNA fingerprinting. J. Clin. Microbiol. 33: 99–102.
- Hiremath, S. S., A. Chowdhary, T. Kowshik, A. H. Randhawa, S. Sun, and J. Xu. 2008. Long-distance dispersal and recombination in environmental populations of Cryptococcus neoformans var. grubii from India. Microbiology 154: 1513–1524.
- Hotzel, H., P. Kielstein, R. Blaschke-Hellmessen, J. Wendisch, and W. Bär. 1998. Phenotypic and genotypic differentiation of several human and avian isolates of Crypto-coccus neoformans . Mycoses 41: 389–396.
- Hunter, P. R., and M. A. Gaston. 1988. Numerical index of the discriminatory ability of typing systems: an application of Simpson's index of diversity. J. Clin. Microbiol. 26: 2465–2466.
- Igreja, R. P., M. S. Lazera, B. Wanke, M. C. G. Galhardo, S. Kidd, and W. Meyer. 2004. Molecular epidemiology of Cryptococcus neoformans isolates from AIDS patients of the Brazilian city, Rio de Janeiro. Med. Mycol. 42: 229–238.
- Karaoglu, H., C. M. Y. Lee, and W. Meyer. 2004. Survey of simple sequence repeats in completed fungal genomes. Mol. Biol. Evol. 22: 639–649.
- Karaoglu, H., C. M. Y. Lee, D. Carter, and W. Meyer. 2008. Development of polymorphic microsatellite markers for Cryptococcus neoformans . Mol. Ecol. Resour. 8: 1136–1138.
- Katsu, M., S. Kidd, A. Ando, M. L. Moretti-Branchini, Y. Mikami, K. Nishimura, and W. Meyer. 2004. The internal transcribed spacers and 5.8S rRNA gene show extensive diversity among isolates of the Cryptococcus neofor-mans species complex. FEMS Yeast Res. 4: 377–388.
- Kidd, S. E., Y. Chow, S. Mak, P. J. Bach, H. Chen, A. O. Hingston, J. W. Kronstad, and K. H. Bartlett. 2007. Characterization of environmental sources of the human and animal pathogen Cryptococcus gattii in British Columbia, Canada and the pacific Northwest of the United States. App. Environ. Microbiol. 73: 1433–1443.
- Kidd, S. E., H. Guo, K. H. Bartlett, J. Xu, and J. W. Kronstad. 2005. Comparative gene genealogies indicate that two clonal lineages of Cryptococcus gattii in British Columbia resemble strains from other geographical areas. Eu-karot. Cell 4: 1629–1638.
- Kidd, S. E., F. Hagen, R. L. Tscharke, M. Huynh, K. H. Bartlett, M. Fyfe, L. MacDougall, T. Boekhout, K. J. Kwon-Chung, and W. Meyer. 2004. A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc. Natl. Acad. Sci. USA 101: 17258–17263.
- Kidd, S. E., C. Hitchcock, K. Maszewska, P. Balakrishnan, C. Hunt, P. Rajendran, A. R. Usha, S. P. Thyagarajan, T. C. Sorrell, and W. Meyer. 2001. Molecular epidemiology of clinical and environmental isolates of Cryptococcus neoformans from Tamil Nadu, India. Australas. Mycol. 20: 105–114.
- Kidd, S. E., T. C. Sorrell, and W. Meyer. 2003. Isolation of two molecular types of Cryptococcus neoformans var. gat-tii from insect frass. Med. Mycol. 41: 171–176.
- Kwon-Chung, K. J. 1975. A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67: 1197–1200.
- Kwon-Chung, K. J. 1976. Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans . Mycologia 68: 821–833.
- Kwon-Chung, K. J. 1976. A new species of Filobasidiella, the sexual state of Cryptococcus neoformans B and C sero-types. Mycologia 68: 943–946.
- Kwon-Chung, K. J., and J. E. Bennett. 1984. Epidemio-logic differences between the two varieties of Cryptococcus neoformans . Am. J. Epidemiol. 120: 123–130.
-
Kwon-Chung, K. J., J. E. Bennett, and T. S. Theodore. 1978.
Cryptococcus bacillisporus sp. nov. serotype B-C of Cryptococcus neoformans
. Int. J. Syst. Bacteriol. 28: 616–620.
10.1099/00207713-28-4-616 Google Scholar
-
Kwon-Chung, K. J., T. Boekhout, J. W. Fell, and M. Diaz. 2002. Proposal to conserve the name Cryptococ-cus gattii against C. hondurianus and C. basillisporus (Basid-iomycota, Hymenomycetes, Tremellomycetidae). Taxon
51: 804–806.
10.2307/1555045 Google Scholar
- Kwon-Chung, K. J., and A. Varma. 2006. Do major species concepts support one, two or more species within Cryptococcus neoformans? FEMS Yeast Res. 6: 574–587.
- Lagrou, K., J. van Eldere, S. Keuleers, F. Hagen, R. Merckx, J. Verhaegen, W. E. Peetermans, and T. Boekhout. 2005. Zoonotic transmission of Cryptococcus neoformans from a magpie to an immunocompetent patient. J. Intern. Med. 257: 385–388.
- Latouche, G. N., M. Huynh, T. C. Sorrell, and W. Meyer. 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.
- Lazéra, M. S., M. A. S. Cavalcanti, A. T. Londero, L. Trilles, M. M. Nishikawa, and B. Wanke. 2000 Possible primary ecological niche of Cryptococcus neoformans. Med. Mycol. 38: 379–383.
- Lemmer, K., D. Naumann, B. Raddatz, and K. Tintelnot. 2004. Molecular typing of Cryptococcus neoformans by PCR fingerprinting, in comparison with serotyping and Fourier transform infrared-spectroscopy-based phenotyp-ing. Med. Mycol. 42: 135–147.
- Levy, R., J. Pitout, P. Long, and M. J. Gill. 2007. Late presentation of Cryptococcus gattii meningitis in a traveller to Vancouver Island: a case report. Can. J. Infect. Dis. Med. Microbiol. 18: 197–199.
- Li, W. H., M. Tanimura, and P. M. Sharp. 1987. An evaluation of the molecular clock hypothesis using mammalian DNA sequences. J. Mol. Evol. 25: 330–342.
- Lindberg, J., F. Hagen, A. Laursen, J. Stenderup, and T. Boekhout. 2007. Cryptococcus gattii risk for tourists visiting Vancouver Island, Canada. Emerg. Infect. Dis. 13: 178–179.
- Litvintseva, A., J. Rosouw, R. Thakur, N. Govender, and T. G. Mitchell. 2008. Cryptococcus neoformans var. grubii (serotype A) in Africa. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-12–03.
- Litvintseva, A. P., L. Kestenbaum, R. Vilgalys, and T. G. Mitchell. 2005. Comparative analysis of environmental and clinical populations of Cryptococcus neoformans . J. Clin. Microbiol. 43: 556–564.
- Litvintseva, A. P., X. Lin, I. Templeton, J. Heitman, and T. G. Mitchell. 2007. Many globally isolated AD hybrid strains of Cryptococcus neoformans originated in Africa. PLoS Pathog. 3:e114.
- Litvintseva, A. P., R. E. Marra, K. Nielsen, J. Heitman, R. Vilgalys, and T. G. Mitchell. 2003. Evidence of sexual recombination among Cryptococcus neoformans serotype A isolates in sub-Saharan Africa. Eukarot. Cell 2: 1162–1168.
- Litvintseva, A. P., R. Thakur, R. Vilgalys, and T. G. Mitchell. 2006. Multilocus sequence typing reveals three genetic subpopulations of Cryptococcus neoformans var. gru-bii (serotype A), including a unique population in Botswana. Genetics 172: 2223–2238.
- MacDougall, L., S. E. Kidd, E. Galanis, S. Mak, M. J. Leslie, P. R. Cieslak, J. W. Kronstad, M. G. Morshed, and K. H. Bartlett. 2007. Spread of Cryptococcus gattii in British Columbia, Canada, and detection in the Pacific Northwest, USA. Emerg. Infect. D is. 13: 42–50.
- Mandal, P., U. Banerjee, A. Casadevall, and J. D. Nosan-chuk. 2005. Dual infections with pigmented and albino strains of Cryptococcus neoformans in patients with and without human immunodeficiency virus infection in India. J. Clin. Microbiol. 43: 4766–4772.
-
Meyer, W., T. G. Mitchell, E. Z. Freedman, and R. Vilgalys. 1993. Hybridization probes for conventional DNA fingerprinting can be used as single primers in the PCR to distinguish strains of Cryptococcus neoformans
. J. Clin. Mi-crobiol. 30: 2274–2280.
10.1128/JCM.31.9.2274-2280.1993 Google Scholar
- Meyer, W., and T. G. Mitchell. 1995. PCR fingerprinting in fungi using single primers specific to minisatellites and simple repetitive DNA sequences: strain variation in Cryp-tococcus neoformans . Electrophoresis 16: 1648–1656.
-
Meyer, W., K. Marszewska, M. Amirmostofian, R. P. Igreja, C. Hardtke, K. Methling, M. A. Viviani, A. Chindamporn, S. Sukroongreung, M. A. John, D. H. Ellis, and T. C. Sorrell. 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.
10.1002/(SICI)1522-2683(19990101)20:8<1790::AID-ELPS1790>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
-
Meyer, W.
2007. The emergence of Cryptococcus gattii VGII as a super killer?
Microbiol. Austral. 5: 70–71.
10.1071/MA07070 Google Scholar
- Meyer, W., D. M. Aanensen, T. Boekhout, M. Cogliati, M. R. Diaz, M. E. Esposto, M. Fisher, F. Gilgado, F. Hagen, S. Kaocharoen, A. P. Litvintseva, T. G. Mitchell, S. P. Simwami, L. Trilles, M. A. Viviani, and J. Kwon-Chung. 2009. Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococ-cus gattii . Med. Mycol. 47: 561–570.
- Meyer, W., A. Castaneda, S. Jackson, M. Huynh, E. Castaneda, and the Ibero-American Cryptococcal Study Group. 2003. Molecular typing of IberoAmerican Crypto-coccus neoformans isolates. Emerg. Infect. Dis. 9: 189–195.
- Meyer, W., F. Gilgado, S. Kaocharoen, L. Trilles, P. Ngamskulrungroj, P. Escandón, F. Hagen, T. Boekhout, A. Chindamporn, and M. S. Lazéra. 2008. Global molecular epidemiology divides the Cryptococcus species complex into 8 major molecular types and reveals the possible origin of the Vancouver Island outbreak. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-12–04.
- Mitchell, T. G., and J. R. Perfect. 1995. Cryptococcosis in the era of AIDS: 100 years after the discovery of Cryptococcus neoformans . Clin. Microbiol. Rev. 8: 515–548.
- Mitchell, T. G., R. L. Sandin, B. H. Bowman, W. Meyer, and W. G. Merz. 1994. Molecular mycology: probes and applications of PCR technology . J. Med. Vet. Mycol. 32 (Suppl. 1): 351–366.
- Miyazaki, Y. 2008. Cryptococcosis in Japan. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-01–04.
- Montagna, M. T. 2002. A note on the isolation of Cryp-tococcus neoformans serotype A MATa strain from the Italian environment. Med. Mycol. 40: 593–595.
- Ngamskulrungroj, P., F. Gilgado, J. Faganello, A. P. Litvntseva, A. L. Leal, K. M. Tsui, T. G. Mitchell, M. H. Vainstein, and W. Meyer. 2009. Genetic diversity of the Cryptococcus species complex suggest that Crypto-coccus gattii deserves to have varieties. PLoS ONE 4 (6): e5862. doi:10.1371/journal.pone.0005862.
- Passoni, L. F. C., B. Wanke, M. M. Nishikawa, and M. S. Lazéra. 1998. Cryptococcus neoformans isolated from human dwellings in Rio de Janeiro, Brazil: an analysis of domestic environment of AIDS patients with and without cryptococcosis. J. Med. Vet. Mycol. 36: 305–311.
- Perfect, J. R., B. B. Magee, and P. T. Magee. 1989. Separation of chromosomes of Cryptococcus neoformans by pulsed field gel electrophoresis. Infect. Immun. 57: 2624–2627.
- Perfect, J. R., N. Ketabchi, G. M. Cox, C. W. Ingram, and C. L. Beiser. 1993. Karyotyping of Cryptococcus neo-formans as an epidemiological tool. J. Clin. Microbiol. 31: 3305–3309.
- Raso, T. F., K. Werther, E. T. Miranda, and M. J. Mendes-Giannini. 2004. Cryptococcosis outbreak in psit-tacine birds in Brazil. Med. Mycol. 42: 355–362.
- Ruma, P., S. C. Chen, T. C. Sorrell, and A. G. Brown-lee. 1996. Characterization of Cryptococcus neoformans by random DNA amplification. Lett. Appl. Microbiol. 23: 312–316.
- Sanfelice, F. 1894. Contributo alla morfologia e biologia dei blastomiceti che si sviluppano nei succhi di alcuni frutti. Ann. Igien. 4: 463–495.
- Saul, N., M. Krockenberger, and D. Carter. 2008. Evidence of recombination in mixed-mating-type and α-only populations of Cryptococcus gattii sourced from single Eucalyptus tree hollows. Eukarot. Cell 7: 727–734.
- Savelkoul, P. H., H. J. Aarts, J. de Haas, L. Dijkshoorn, B. Duim, M. Otsen, J. L. Rademaker, L. Schouls, and J. A. Lenstra. 1999. Amplified-fragment length polymorphism analysis: the state of an art. J. Clin. Microbiol. 37: 3083–3091.
- Schwarz, D. C., and C. R. Cantor. 1984. Separation of yeast chromosome-sized DNAs by pulsed field gradient gel electrophoresis. Cell 37: 67–75.
- Sharpton, T. J., D. E. Neafsey, J. E. Galagan, and J. W. Taylor. 2008. Mechanisms of intron gain and loss in Cryptococcus . Genome Biol. 9:R24.
- Simpson, E. H. 1949. Measurement of diversity. Nature 163 6–88.
- Soll, D. R. 2000. The ins and outs of DNA fingerprinting the infectious fungi. Clin. Microbiol. Rev. 13: 332–370.
- Sorrell, T. C., S. C. Chen, P. Ruma, W. Meyer, T. J. Pfeiffer, D. H. Ellis, and A. G. Brownlee. 1996. Concordance of clinical and environmental isolates of Cryp-tococcus neoformans var. gattii by random amplification of polymorphic DNA analysis and PCR fingerprinting. J. Clin. Microbiol. 34: 1253–1260.
- Sorrell, T. C., A. G. Brownlee, P. Ruma, R. Malik, T. J. Pfeiffer, and D. H. Ellis. 1996. Natural environmental sources of Cryptococcus neoformans var. gattii . J. Clin. Microbiol. 34: 1261–1263.
- Spitzer, E. D., and S. G. Spitzer. 1992. Use of a dispersed repetitive DNA element to distinguish clinical isolates of Cryptococcus neoformans . J. Clin. Microbiol. 30: 1094–1097.
- St-Germain, G., G. Noel, and K. J. Kwon-Chung. 1988. Disseminated cryptococcosis due to Cryptococcus neofor-mans var. gattii in a Canadian patient with AIDS. Eur. J. Clin. Microbiol. Infect. Dis. 7: 587–588.
- Sugita, T., R. Ikeda, and T. Shinoda. 2001. Diversity among strains of Cryptococcus neoformans var. gattii as revealed by a sequence analysis of multiple genes and a che-motype analysis of capsular polysaccharide. Microbiol. Immunol. 45: 757–768.
- Supparatpinyo, K. 2008. Cryptococcosis in Thailand. 7th International Conference on Cryptococcus & Crypto-coccosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-01–05.
- Swinne, D., M. Deppner, R. Laroche, J. J. Floch, and P. Kadende. 1989. Isolation of Cryptococcus neoformans from houses of AIDS-associated cryptococcosis patients in Bujumbura (Burundi). AIDS 3: 389–390.
- Tautz, D., and M. Renz. 1984. Simple sequences are ubiquitous repetitive components of eukaryotic genomes. Nucleic Acids Res. 12: 4127–4138.
- Taylor, J. W., and M. C. Fisher. 2003. Fungal multi-locus sequence typing: it's not just for bacteria. Curr. Opin. Microbiol. 6: 1–6.
- Trilles, L., M. S. Lazéra, B. Wanke, B. Theelen, and T. Boekhout. 2003. Genetic characterization of environmental isolates of the Cryptococcus neoformans species complex from Brazil. Med. Mycol. 41: 383–390.
- Trilles, L., M. S. Lazéra, B. Wanke, R. V. Oliveira, G. G. Barbosa, M. M. Nishikawa, B. P. Morales, and W. Meyer. 2008. Regional pattern of the molecular types of Cryptococcus neoformans and Cryptococcus gattii in Brazil. Mem. Inst. Oswaldo Cruz 103: 455–462.
- Upton, A., J. A. Fraser, S. E. Kidd, C. Bretz, K. H. Bartlett, J. Heitman, and K. A. Marr. 2007. First contemporary case of human infection with Cryptococus gattii in Puget Sound: evidence of spread of the Vancouver Island outbreak. J. Clin. Microbiol. 45: 3086–3088.
- Vanbreuseghem, R., and M. Takashio. 1970. An atypical strain of Cryptococcus neoformans (Sanfelice) Vuillemin. 1894, II. Cryptococcus neoformans var. gattii var. nov. Ann. Soc. Belg. Med. Trop. 50: 695–702.
- Varma, A., and K. J. Kwon-Chung. 1989. Restriction fragment polymorphism in mitochondrial DNA of Cryp-tococcus neoformans . J. Gen. Microbiol. 135: 3353–3362.
- Varma, A., and K. J. Kwon-Chung. 1992. DNA probe for strain typing of Cryptococcus neoformans . J. Clin. Mi-crobiol. 30: 2960–2967.
- Varma, A., D. Swinne, F. Staib, J. E. Bennett, and K. J. Kwon-Chung. 1995. Diversity of DNA fingerprint-ing in Cryptococcus neoformans . J. Clin. Microbiol. 33: 1807–1814.
- Velegraki, A., V. G. Kiosses, A. Kansouzidou, S. Smi-lakou, A. Mitroussia-Ziouva, and N. J. Legakis. 2001. Prospective use of RFLP analysis on amplified Cryptococcus neoformans URA5 gene sequences for rapid identification of varieties and serotypes in clinical samples. Med. Mycol. 39: 409–417.
- Vilgalys, R., and M. Hester. 1990. Rapid genetic identification and mapping of enzymatically amplified ribo-somal DNA from several Cryptococcus species. J. Bacte-riol. 172: 4238–4246.
- Viviani, M. A., M. Cogliati, M. C. Esposto, K. Lemmer, K. Tintelnot, M. F. C. Valiente, D. Swinne, A. Velegraki, R. Velho, and the European Confederation of Medical Mycology (ECMM) Cryptococcosis Working Group. 2006. Molecular analyses of 311 Cryptococcus neoformans isolates from a 30-month ECMM survey of cryptococcosis in Europe. FEMS Yeast Res. 6: 614–619.
- Viviani, M. A., M. C. Esposto, M. Cogliati, M. T. Montagna, and B. L. Wickes. 2001. Isolation of a Cryptococcus neoformans serotype A MAT a strain from the Italian environment. Med. Mycol. 39: 383–386.
- Viviani, M. A., H. Wen, A. Roverselli, R. Caldarelli-Stefano, M. Cogliati, P. Ferrante, A. M. Tortorano. 1997. Identification by polymerase chain reaction finger-printing of Cryptococcus neoformans serotype AD. J. Med. Vet. Mycol. 35: 355–360.
- Vos, P., R. Hogers, M. Bleeker, M. Reijans, T. van de Lee, M. Hornes, A. Frijters, J. Pot, J. Peleman, M. Kui-per, and M. Zabeau. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407–4414.
- Wickes, B. L., T. D. E. Moore, and K. J. Kwon-Chung. 1994. Comparison of the electrophoretic karyotypes and chromosomal location of ten genes in the two varieties of Cryptococcus neoformans . Microbiology 140: 543–550.
- Williams, J. G. K., A. R. Kubelik, K. J. Livak, J. A. Raflski, S. V. Tingey. 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res. 18: 6532–6535.
- Woo, J. H. 2008. Prognostic factors of cryptococcal men-ingitisin patients without HIV infection. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-01–02.
- Xu, J., R. Vilgalys, and T. G. Mitchell. 2000. Multiple gene genealogies reveal recent dispersion and hybridization in the human pathogenic fungus Cryptococcus neofor-mans . Mol. Ecol. 9: 1471–1481.
- Yamamoto, Y., S. Kohno, H. Koga, H. Kakeya, K. To-mono, M. Kaku, T. Yamazaki, M. Arisawa, and K. Hara. 1995. Random amplified polymorphic DNA analysis of clinically and environmentally isolated Cryptococcus neo-formans in Nagasaki. J. Clin. Microbiol. 33: 3328–3332.
- Yuanjie, Z., W. Hai, C. Jianhan, and G. Julin. 2008. Mycological profile of HIV-negative patients with cryptococcal meningitis during treatment and after follow-up. 7th International Conference on Cryptococcus & Crypto-coccosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-01–03.
- Zue, L. P., B. Xu, J. Q. Wu, X. T. Ou, Q. Q. Zhang, and X. H. Weng. 2008. Cryptococcal meningitis in non-HIV patients: review of 11 years experience in a Chinese tertiary care hospital. 7th International Conference on Cryptococcus & Cryptococcosis, Nagasaki, Japan, 11 to 14 September 2008, abstract #SY-03–02.