Morphological and genomic characterization of Filobasidiella depauperata: a homothallic sibling species of the pathogenic cryptococcus species complex.

Marianela Rodriguez-Carres,Fred S Dietrich,Joseph Heitman,Sheng Sun,Keisha Findley

doi:10.1371/journal.pone.0009620

Marianela Rodriguez-Carres, Fred S Dietrich + Show 3 more

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https://doi.org/10.1371/journal.pone.0009620

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Journal: PloS one	Publication Date: Mar 10, 2010
Citations: 88	License type: CC BY 4.0

Affiliation: Duke University Hospital, Duke Medical Center

Abstract

The fungal species Cryptococcus neoformans and Cryptococcus gattii cause respiratory and neurological disease in animals and humans following inhalation of basidiospores or desiccated yeast cells from the environment. Sexual reproduction in C. neoformans and C. gattii is controlled by a bipolar system in which a single mating type locus (MAT) specifies compatibility. These two species are dimorphic, growing as yeast in the asexual stage, and producing hyphae, basidia, and basidiospores during the sexual stage. In contrast, Filobasidiella depauperata, one of the closest related species, grows exclusively as hyphae and it is found in association with decaying insects. Examination of two available strains of F. depauperata showed that the life cycle of this fungal species shares features associated with the unisexual or same-sex mating cycle in C. neoformans. Therefore, F. depauperata may represent a homothallic and possibly an obligately sexual fungal species. RAPD genotyping of 39 randomly isolated progeny from isolate CBS7855 revealed a new genotype pattern in one of the isolated basidiospores progeny, therefore suggesting that the homothallic cycle in F. depauperata could lead to the emergence of new genotypes. Phylogenetic analyses of genes linked to MAT in C. neoformans indicated that two of these genes in F. depauperata, MYO2 and STE20, appear to form a monophyletic clade with the MAT a alleles of C. neoformans and C. gattii, and thus these genes may have been recruited to the MAT locus before F. depauperata diverged. Furthermore, the ancestral MAT a locus may have undergone accelerated evolution prior to the divergence of the pathogenic Cryptococcus species since several of the genes linked to the MAT a locus appear to have a higher number of changes and substitutions than their MATα counterparts. Synteny analyses between C. neoformans and F. depauperata showed that genomic regions on other chromosomes displayed conserved gene order. In contrast, the genes linked to the MAT locus of C. neoformans showed a higher number of chromosomal translocations in the genome of F. depauperata. We therefore propose that chromosomal rearrangements appear to be a major force driving speciation and sexual divergence in these closely related pathogenic and saprobic species.

Highlights

Previous studies have shown that selective forces promote clustering of genes that are co-expressed because they are involved in the same biosynthetic pathway or developmental process
In the basidiomycetous yeasts C. neoformans and C. gattii mating is controlled by a bipolar mating system in which a single mating type locus (MAT) locus contains the pheromone/pheromone receptor genes linked to the genes encoding the homeodomain proteins [6]
The 2% sequence differences between the elongation factor 1 alpha (EF1a) and RPB1 genes in F. depauperata appear to be the result of transitions and synonymous substitutions, consistent with recent divergence of the two strains

Summary

Introduction

Previous studies have shown that selective forces promote clustering of genes that are co-expressed because they are involved in the same biosynthetic pathway or developmental process. It has been postulated that the sex-determining locus of the human pathogenic fungi C. neoformans and C. gattii were shaped by genomic events similar to those that drove the evolution of sex chromosomes in mammals, including sequential gene acquisitions, suppression of recombination, and chromosomal rearrangements [2]. Sexual reproduction is determined by compatibility at the MAT locus. In the basidiomycetous yeasts C. neoformans and C. gattii mating is controlled by a bipolar mating system in which a single MAT locus contains the pheromone/pheromone receptor genes linked to the genes encoding the homeodomain proteins [6]. Under laboratory conditions sexual reproduction is triggered in these fungi by the recognition of a compatible mating partner that usually carries a different MAT allele (MATa and MATa). Basidiospores subsequently germinate into yeast cells that divide mitotically by budding, initiating the asexual stage of the life cycle

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