The human fungal pathogen Paracoccidioides brasiliensis (Onygenales: Ajellomycetaceae) is a complex of two species: Phylogenetic evidence from five mitochondrial markers

Cladistics

Volumn 26, Issue 6, 2010, Pages 613-624

  Salgado Salazar, Catalina ^a,b   Jones, Leandro R ^c,d   Restrepo, Ángela ^a   McEwen, Juan G ^a,b  

^a Corporación Para Investigaciones Biológicas ^*  (Colombia)

^b UNIVERSIDAD DE ANTIOQUIA   (Colombia)

^c Estacion de Fotobiologia Playa Union   (Argentina)

^d UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BAYESIAN ANALYSIS; DATA SET; ETIOLOGY; FUNGAL DISEASE; FUNGUS; GENETIC ANALYSIS; GENETIC MARKER; GEOGRAPHICAL VARIATION; MITOCHONDRION; NEW SPECIES; PATHOGEN; PHYLOGENETICS; SPECIES COMPLEX; TAXONOMY;

LATIN AMERICA;

AJELLOMYCETACEAE; NEUROSPORA CRASSA; ONYGENALES; PARACOCCIDIOIDES; PARACOCCIDIOIDES BRASILIENSIS;

EID: 78349247942     PISSN: 07483007     EISSN: 10960031     Source Type: Journal    
DOI: 10.1111/j.1096-0031.2010.00307.x     Document Type: Article

References (69)

1. Albuquerque, P., Kyaw, C.M., Saldanha, R.R., Brigido, M.M., Felipe, M.S., Silva-Pereira, I., 2004. Pbhyd1 and Pbhyd2: two mycelium-specific hydrophobin genes from the dimorphic fungus Paracoccidioides brasiliensis. Fungal Genet. Biol. 41, 510-520.
2. Almeida, A.J., Matute, D.R., Carmona, J.A., Martins, M., Torres, I., McEwen, J.G., Restrepo, A., Leao, C., Ludovico, P., Rodrigues, F., 2007. Genome size and ploidy of Paracoccidioides brasiliensis reveals a haploid DNA content: flow cytometry and GP43 sequence analysis. Fungal Genet. Biol. 44, 25-31.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
4. Andrew, M., Peever, T.I., Pryor, B.M., 2009. An expanded multilocus phylogeny does not resolve morphological species within the small-spored Alternaria species complex. Mycologia 101, 95-109.
5. Barbosa, M.S., Cunha Passos, D.A., Felipe, M.S., Jesuíno, R.S., Pereira, M., De Almeida Soares, C.M., 2004. The glyceraldehyde-3-phosphate dehydrogenase homologue is differentially regulated in phases of Paracoccidioides brasiliensis: molecular and phylogenetic analysis. Fungal Genet. Biol. 41, 667-675.
6. Batista, W.L., Barros, T.F., Goldman, G.H., Morais, F.V., Puccia, R., 2007. Identification of transcription elements in the 5' intergenic region shared by LON and MDJ1 heat shock genes from the human pathogen Paracoccidioides brasiliensis. Evaluation of gene expression. Fungal Genet. Biol. 44, 47-56.
7. Biswas, S.K., Yokoyama, K., Nishimura, K., Miyaji, M., 2001. Molecular phylogenetics of the genus Rhodotorula and related basidiomycetous yeast inferred from the mitochondrial cytochrome b gene. Int. J. Syst. Evol. Microbiol. 51, 1191-1199.
8. Bonfim, S.M., Cruz, A.H., Jesuino, R.S., Ulhoa, C.J., Molinari-Madlum, E.E., Soares, C.M., Pereira, M., 2006. Chitinase from Paracoccidioides brasiliensis: molecular cloning, structural, phylogenetic, expression and activity analysis. FEMS Immunol. Med. Microbiol. 46, 269-283.
9. Borges-Walmsley, M.I., Chen, D., Shu, X., Walmsley, A.R., 2002. The pathobiology of Paracoccidioides brasiliensis. Trends Microbiol. 10, 80-87.
10. Bremer, K., 1990. Combinable component consensus. Cladistics 6, 369-372.
11. Brummer, E., Castañeda, E., Restrepo, A., 1993. Paracoccidioidomycosis: an update. Clin. Microbiol. Rev. 6, 89-117.
12. Burke, J.M., Breitenberger, C., Heckman, J.E., Dujon, B., Rajbhandary, U.L., 1984. Cytochrome b gene of Neurospora crassa mitochondria. Partial sequence and location of introns at sites different from those in Saccharomyces cerevisiae and Aspergillus nidulans. J. Biol. Chem. 259, 504-511.
13. Calcagno, A.M., Nino-Vega, G., San-Blas, F., San-Blas, G., 1998. Geographic discrimination of Paracoccidioides brasiliensis strains by randomly amplified polymorphic DNA analysis. J. Clin. Microbiol. 36, 1733-1736.
14. Cardoso, M.A., Tambor, J.H., Nobrega, F.G., 2007. The mitochondrial genome from the thermal dimorphic fungus Paracoccidioides brasiliensis. Yeast 24, 607-616.
15. Carrero, L.L., Niño-Vega, G., Teixeira, M.M., Carvalho, M.J.A., Soares, C.M.A., Pereira, M., Jesuino, R.S.A., McEwen, J.G., Mendosa, L., Taylor, J.W., Felipe, M.S., San-Blas, G., 2008. New Paracoccidioides brasiliensis isolate reveals unexpected genomic variability in this human pathogen. Fungal Genet. Biol. 45, 605-612.
16. Carvalho, K.C., Ganiko, L., Batista, W., Morais, F.V., Marques, E.R., Goldman, G.H., Franco, M.F., Puccia, R., 2005. Virulence of Paracoccidioides brasiliensis and gp43 expression in isolates bearing known PbGP43 genotype. Microbes Infect. 7, 55-65.
17. Correa, M.M., Bedoya, A.M., Guerrero, M.P., Mendez, J., Restrepo, A., McEwen, J.G., 2006. Diagnosis of paracoccidioidomycosis by a dot blot assay using a recombinant Paracoccidioides brasiliensis p27 protein. Mycoses 50, 41-47.
18. Dettman, J.R., Jacobson, D.J., Taylor, J.W., 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57, 2703-2720.
19. Diez, S., Garcia, E.A., Pino, P.A., Botero, S., Corredor, G.G., Peralta, L.A., Castaño, J.H., Restrepo, A., McEwen, J.G., 1999. PCR with Paracoccidioides brasiliensis specific primers: potential use in ecological studies. Rev. Inst. Med. Trop. Sao Paulo 41, 351-358.
20. Farris, J.S., 1989. The retention index and homoplasy excess. Syst. Biol. 38, 406-407.
21. Goldman, G.H., Dos Reis Marques, E., Duarte Ribeiro, D.C., De Souza Bernardes, L.A., Quiapin, A.C., Vitorelli, P.M., Savoldi, M., Semighini, C.P., De Oliveira, R.C., Nunes, L.R., Travassos, L.R., Puccia, R., Batista, W.L., Ferreira, L.E., Moreira, J.C., Bogossian, A.P., Tekaia, F., Nobrega, M.P., Nobrega, F.G., Goldman, M.H., 2003. Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryot. Cell 2, 34-48.
22. Goloboff, P.A., 1999. Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15, 415-428.
23. Goloboff, P., 2007. Calculating SPR distances between trees. Cladistics 23, 1-7.
24. Goloboff, P.A., Farris, J.S., 2001. Methods for quick consensus estimations. Cladistics 17, S26-S34.
25. Goloboff, P., Farris, J.S., Nixon, K. 2003a. T.N.T.: Tree Analysis Using New Technology. Program and documentation available from the authors and at
26. Goloboff, P.A., Farris, J.S., Källersjo, M., Oxelman, B., Ramirez, M., Szumik, C., 2003b. Improvements to resampling measures of group support. Cladistics 19, 324-332.
27. Goloboff, P.A., Farris, J.S., Nixon, K.C., 2008. TNT, a free program for phylogenetic analysis. Cladistics 24, 774-786.
28. Gray, M.W., 1989. Origin and evolution of mitochondrial DNA. Annu. Rev. Cell Biol. 5, 25-50.
29. Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755.
30. Huelsenbeck, J.P., Ronquist, F., 2005. Bayesian analysis of molecular evolution using MrBayes. In: Nielsen, R. (Ed.), Statistical Methods in Molecular Evolution. Springer, New York, pp. 183-226.
31. Kluge, A., Farris, J., 1969. Quantitative phyletics and the evolution of Anurans. Syst. Zool. 18, 1-32.
32. Kouvelis, V.N., Ghikas, D.V., Typas, M.A., 2004. The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of Sordariomycetes: phylogenetic implications. Fungal Genet. Biol. 41, 930-940.
33. Kurokawa, C.S., Lopes, C.R., Sugizaki, M.F., Kuramae, E.E., Franco, M.F., Peraçoli, M.T., 2005. Virulence profile of ten Paracoccidioides brasiliensis isolates: association with morphologic and genetic patterns. Rev. Inst. Med. Trop. Sao Paulo 47, 257-262.
34. Lang, B.F., Ahne, F., Bonen, L., 1985. The mitochondrial genome of the fission yeast Schizosaccharomyces pombe. The cytochrome b gene has an intron closely related to the first two introns in the Saccharomyces cerevisiae cox1 gene. J. Mol. Biol. 184, 353-366.
35. Leclerc, M.C., Philippe, H., Gueho, E., 1994. Phylogeny of dermatophytes and dimorphic fungi based on large subunit ribosomal RNA sequence comparisons. J. Med. Vet. Mycol. 32, 331-341.
36. Marques-da-Silva, S.H., Colombo, A.L., Blotta, M.H., Queiroz-Telles, F., Balthazar, A.B., Lopes, J.D., De Camargo, Z.P., 2006. Diagnosis of Paracoccidioidomycosis by detection of antigen and antibody in bronchoalveolar lavage fluids. Clin. Vaccine Immunol. 13, 1363-1366.
37. Matute, D.R., McEwen, J.G., Puccia, R., Montes, B.A., San-Blas, G., Bagagli, E., Rauscher, J.T., Restrepo, A., Morais, F., Nino-Vega, G., Taylor, J.W., 2006a. Cryptic speciation and recombination in the fungus Paracoccidioides brasiliensis as revealed by gene genealogies. Mol. Biol. Evol. 23, 65-73.
38. Matute, D.R., Sepulveda, V.E., Quesada, L.M., Goldman, G.H., Taylor, J.W., Restrepo, A., McEwen, J.G., 2006b. Microsatellite analysis of three phylogenetic species of Paracoccidioides brasiliensis. J. Clin. Microbiol. 44, 2153-2157.
39. Matute, D.R., Torres, I.P., Salgado-Salazar, C., Restrepo, A., McEwen, J.G., 2007. Background selection at the chitin synthase II (chs2) locus in Paracoccidioides brasiliensis species complex. Fungal Genet. Biol. 44, 357-367.
40. Matute, D.R., Quesada-Ocampo, L.M., Rauscher, J.T., McEwen, J.G., 2008. Evidence for positive selection in putative virulence factors within the Paracoccidioides brasiliensis species complex. PLoS Negl. Trop. Dis. 2, e296.
41. McEwen, J.G., Bedoya, V., Patiño, M.M., Salazar, M.E., Restrepo, A., 1987. Experimental murine paracoccidioidomycosis induced by the inhalation of conidia. J. Med. Vet. Mycol. 25, 165-175.
42. McEwen, J.G., Garcia, A.M., Ortiz, B.L., Botero, S., Restrepo, A., 1995. In search of the natural habitat of Paracoccidioides brasiliensis. Arch. Med. Res. 26, 305-306.
43. Molinari-Madlum, E.E., Felipe, M.S., Soares, C.M., 1999. Virulence of Paracoccidioides brasiliensis isolates can be correlated to groups defined by random amplified polymorphic DNA analysis. Med. Mycol. 37, 269-276.
44. Morais, F.V., Barros, T.F., Fukada, M.K., Cisalpino, P.S., Puccia, R., 2000. Polymorphism in the gene coding for the immunodominant antigen gp43 from the pathogenic fungus Paracoccidioides brasiliensis. J. Clin. Microbiol. 38, 3960-3986.
45. Nascimento, E., Martinez, R., Lopes, A.R., De Souza, L.A., Barco, C.P., Goldman, M.H., Taylor, J.W., McEwen, J.G., Nobrega, M.P., Nobrega, F.G., Goldman, G.H., 2004. Detection and selection of microsatellites in the genome of Paracoccidioides brasiliensis as molecular markers for clinical and epidemiological studies. J. Clin. Microbiol. 42, 5007-5014.
46. Nino-Vega, G., Calcagno, A.M., San-Blas, G., San-Blas, F., Gooday, G.W., Gow, N.A.R., 2000. RFLP analysis reveals marked geographical isolation between strains of Paracoccidioides brasiliensis. Med. Mycol. 38, 437-441.
47. Nino-Vega, G., Perez-Silva, C., San-Blas, G., 2007. The actin gene in P. brasiliensis: organization, expression and phylogenetic analyses. Mycol. Res. 111, 363-369.
48. Nylander, J.A., 2004. MrAIC.pl. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
49. Paradis, E., Claude, J., Strimmer, K., 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290.
50. Philippe, H., Snell, E., Bapteste, E., Lopez, P., Holland, P., Casane, D., 2004. Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol. Biol. Evol. 21, 1740-1752.
51. Printzen, C.E., Stefan, E., 2003. Local population subdivision in the lichen Cladonia subcervicornis as revealed by mitochondrial cytochrome oxidase subunit 1 intron sequences. Mycologia 95, 399-406.
52. Rambaut, A., Drummond, A.J., 2007. Tracer v1.4. Available from
53. Rekab, D., Del Sorbo, G., Reggio, C., Zoina, A., Firrao, G., 2004. Polymorphisms in nuclear rDNA and mtDNA reveal the polyphyletic nature of isolates of Phomopsis pathogenic to sunflower and a tight monophyletic clade of defined geographic origin. Mycol. Res. 108, 393-402.
54. Restrepo, A., Tobon, A., 2005. Paracoccidioides brasiliensis. In: Mandell, G.L., Bennett, J.E., Dollin, R. (Eds.), Principles and Practice of Infectious Diseases. Elsevier, Philadelphia, pp. 3062-3068.
55. Restrepo-Moreno, A., 2003. Paracoccidioidomycosis. In: Dismukes, W.E., Pappas, P.G., Sobel, J.D. (Eds.), Clinical Mycology. Oxford University Press, Oxford, pp. 328-345.
56. San-Blas, G., Prieto, A., Bernabé, M., Ahrazem, O., Moreno, B., Leal, J.A., 2005. alpha-galf I→6-alpha-mannopyranoside side chains in Paracoccidioides brasiliensis cell wall are shared by members of the Onygenales, but not by galactomannans of other fungal genera. Med. Mycol. 43, 153-159.
57. Seraphin, B., Boulet, A., Simon, M., Faye, G., 1987. Construction of a yeast strain devoid of mitochondrial introns and its use to screen nuclear genes involved in mitochondrial splicing. Proc. Natl Acad. Sci. USA 84, 6810-6814.
58. Smith, S.W., Overbeek, R., Woese, C.R., Gilbert, W., Gillevet, P.M., 1994. The genetic data environment an expandable GUI for multiple sequence analysis. Comput. Appl. Biosci. 10, 671-675.
59. Steel, M., Dress, A.W.M., Bocker, S., 2000. Simple but fundamental limitations on supertree and consensus tree methods. Syst. Biol. 49, 363-368.
60. Tambor, J.H.M., Guedes, R.F., Nobrega, M.P., Nobrega, F.G., 2006. The complete DNA sequence of the mitochondrial genome of the dermatophyte fungus Epidermophyton floccosum. Curr. Genet. 49, 302-308.
61. Taylor, J.W., Jacobson, D.J., Kroken, S., Kasuga, T., Geiser, D.M., Hibbett, D.S., Fisher, M.C., 2000. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31, 21-32.
62. Teixeira, M.M., Theodoro, R.C., De Carvalho, M.J.A., Fernandes, L., Paes, H.C., Hahn, R.C., Mendoza, L., Bagagli, E., San-Blas, G., Felipe, M.S.S., 2009. Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol. Phylogenet. Evol. 52, 273-283.
63. Theodoro, R.C., Bagagli, E., Oliveira, C., 2008a. Phylogenetic analysis of PRP8 intein in Paracoccidioides brasiliensis species complex. Fungal Genet. Biol. 45, 1284-1291.
64. Theodoro, R.C., De Moraes Gimenes, B.S., Araújo, J.P., Candeias, J.M., Da Graça Macoris, S.A., Trinca, L.A., Bagagli, E., 2008b. Dimorphism, thermal tolerance, virulence and heat shock protein 70 transcription in different isolates of Paracoccidioides brasiliensis. Mycopathologia 165, 355-365.
65. Thompson, J.D., Higgins, D.G., Gibson, T.J., 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.
66. Untereiner, W.A., Scott, J.A., Naveau, F.A., Currah, R.S., Bachewich, J., 2002. Phylogeny of Ajellomyces, Polytolypa and Spiromastix (Onygenaceae) inferred from the analysis of rDNA sequence and non-molecular data. Stud. Mycol. 47, 25-35.
67. Van Burik, J.A., Schreckhise, R.W., White, T.C., Bowden, R.A., Myerson, D., 1998. Comparison of six extraction techniques for isolation of DNA from filamentous fungi. Med. Mycol. 36, 299-303.
68. Wiens, J.J., 2006. Missing data and the design of phylogenetic analyses. J. Biomed. Inform. 39, 34-42.
69. Zacharias, D., Ueda, A., Moscardi-Bacchi, M., Franco, M., San-Blas, G., 1986. A comparative histopathological, immunological, and biochemical study of experimental intravenous paracoccidioidomycosis induced in mice by three Paracoccidioides brasiliensis isolates. J. Med. Vet. Mycol. 24, 445-454.