Cryptic Speciation and Recombination in the Fungus Paracoccidioides brasiliensis as Revealed by Gene Genealogies

Abstract

Paracoccidioides brasiliensis is the etiologic agent of paracoccidioidomycosis, a disease confined to Latin America and of marked importance in the endemic areas due to its frequency and severity. This species is considered to be clonal according to mycological criteria and has been shown to vary in virulence. To characterize natural genetic variation and reproductive mode in this fungus, we analyzed P. brasiliensis phylogenetically in search of cryptic species and possible recombination using concordance and nondiscordance of gene genealogies with respect to phylogenies of eight regions in five nuclear loci. Our data indicate that this fungus consists of at least three distinct, previously unrecognized species: S1 (species 1 with 38 isolates), PS2 (phylogenetic species 2 with six isolates), and PS3 (phylogenetic species 3 with 21 isolates). Genealogies of four of the regions studied strongly supported the PS2 clade, composed of five Brazilian and one Venezuelan isolate. The second clade, PS3, composed solely of 21 Colombian isolates, was strongly supported by the alpha-tubulin genealogy. The remaining 38 individuals formed S1. Two of the three lineages of P. brasiliensis, S1 and PS2, are sympatric across their range, suggesting barriers to gene flow other than geographic isolation. Our study provides the first evidence for possible sexual reproduction in P. brasiliensis S1, but does not rule it out in the other two species.

Paracoccidioides brasiliensis: chemical and molecular tools for research on cell walls, antifungals, diagnosis, taxonomy

“…Our results [Carrero et al submitted] indicated that a particular isolate (Pb01) was basal and distant to all other isolates. Moreover, the genetic variation in coding regions of P. brasiliensis indicates that there may be more than the three phylogenetic species already reported in the morphological species P. brasiliensis [57]. Strain Pb01 is of interest, because this particular isolate is so far, the best studied isolate from a molecular point of view, as deduced from a thorough analysis of its transcriptome, that yielded 6,022 assembled groups from mycelium and yeast phase expressed sequence tags, covering about 80% of the estimated P. brasiliensis Pb01 genome [58].…”

“…Based on phylogenetic analysis of 65 P. brasiliensis isolates, Matute et al [57] recently proposed three distinct phylogenetic species within P. brasiliensis: S1 (a paraphyletic group formed by 38 isolates of Argentinean, Brazilian, Peruvian and Venezuelan origins, plus an isolate from an Antarctic penguin), PS2 (six isolates, five of them of Brazilian origin, and one Venezuelan) and PS3 (21 Colombian isolates).…”

“…Following this line of research, we analyzed the phylogenetic relationship of coding and non-coding regions of various genes (CHS4, Actin, ODC, URA3, CHS2, HSP70, FKS1, Hidrophobin, Kex1, Catalase A, Catalase P, Formamidase, Glyoxalase and ITS) in 21 P. brasiliensis isolates, 9 of which had not been included in the previous study [57]. Our results [Carrero et al submitted] indicated that a particular isolate (Pb01) was basal and distant to all other isolates.…”

Paracoccidioides brasiliensis: phylogenetic and ecological aspects

“…Consequently, the failure to detect sexual structure does not signify the absence of such structures. Using this approach, Matute et al [84,85] were able to detect three cryptic species in P. brasiliensis, from which two are phylogenetic species (PS2, composed of Brazilian and Venezuelan isolates, and PS3, restricted to Colombia) and one is a paraphyletic species (S1, which has a wider habitat range across the endemic areas). They also observed that while S1 and PS2 were considered recombining sexual species, PS3 was shown to be clonal.…”

Inteins in pathogenic fungi: a phylogenetic tool and perspectives for therapeutic applications

“…This method also provides information about the reproductive mode of the different divergent species, even without the isolation of sexual structures. Cryptic species have been detected by gene genealogies in important pathogenic fungi, such as C. immitis (separated into 2 species: C. immitis and C. posadasii) (Koufopanou et al 2001), H. capsulatum (separated into at least 7 species) (Kasuga et al 2003) and P. brasiliensis, which is now separated into at least four previously unrecognized species: S1 (species 1 from Brazil, Argentina, Paraguay, Peru and Venezuela), PS2 (phylogenetic species 2 from Brazil and Venezuela), PS3 (phylogenetic species 3 with 21 isolates from Colombia) (Matute et al 2006) and Pb01-like (from the central region of Brazil) (Carrero et al 2008, Teixeira 2008.…”