Genomic and Population Analyses of the Mating Type Loci in Coccidioides Species Reveal Evidence for Sexual Reproduction and Gene Acquisition

Abstract

Coccidioides species, the fungi responsible for the valley fever disease, are known to reproduce asexually through the production of arthroconidia that are the infectious propagules. The possible role of sexual reproduction in the survival and dispersal of these pathogens is unexplored. To determine the potential for mating of Coccidioides, we analyzed genome sequences and identified mating type loci characteristic of heterothallic ascomycetes. Coccidioides strains contain either a MAT1-1 or a MAT1-2 idiomorph, which is 8.1 or 9 kb in length, respectively, the longest reported for any ascomycete species. These idiomorphs contain four or five genes, respectively, more than are present in the MAT loci of most ascomycetes. Along with their cDNA structures, we determined that all genes in the MAT loci are transcribed. Two genes frequently found in common sequences flanking MAT idiomorphs, APN2 and COX13, are within the MAT loci in Coccidioides, but the MAT1-1 and MAT1-2 copies have diverged dramatically from each other. Data indicate that the acquisition of these genes in the MAT loci occurred prior to the separation of Coccidioides from Uncinocarpus reesii. An analysis of 436 Coccidioides isolates from patients and the environment indicates that in both Coccidioides immitis and C. posadasii, there is a 1:1 distribution of MAT loci, as would be expected for sexually reproducing species. In addition, an analysis of isolates obtained from 11 soil samples demonstrated that at three sampling sites, strains of both mating types were present, indicating that compatible strains were in close proximity in the environment.

Recent Advances in Our Understanding of the Environmental, Epidemiological, Immunological, and Clinical Dimensions of Coccidioidomycosis

“…Their closest relative for which a genome sequence is currently published, determined by both phylogenetic analysis and morphology, is Uncinocarpus reesii (Onygenaceae), a keratinophilic saprotroph (6,7). Whereas U. reesii has a known sexual life cycle (7,8), the sexual cycle of Coccidioides remains undescribed. No other dimorphic pathogens of humans have been described in the Onygenaceae family (7,9,10).…”

Both mating types in the heterothallic fungus Ophiostoma quercus contain MAT1-1 and MAT1-2 genes

“…Also, the availability of information on the mating idiomorphs allowed for the assessment of the presence of MAT genes in the genome of apparently asexual species (Foster and Fitt 2003;Mandel et al 2007;Turgeon 1998). At the intraspecies level, knowledge regarding the distribution of MAT genes has also shed light on the preferred reproduction mode (i.e.…”

The Evolution of Sex: a Perspective from the Fungal Kingdom

“…Sexual reproduction has been described for H. capsulatum (142,146), B. dermatitidis (194), and most dermatophyte species (307). While successful mating has not yet been observed for P. marneffei, C. immitis, or C. posadasii, genes related to sexual reproduction have been identified in the genomes of these dimorphic fungal species (70,189,311). Data from population genetic studies also support extant sexual reproduction (30,61,62,138,189).…”

“…While successful mating has not yet been observed for P. marneffei, C. immitis, or C. posadasii, genes related to sexual reproduction have been identified in the genomes of these dimorphic fungal species (70,189,311). Data from population genetic studies also support extant sexual reproduction (30,61,62,138,189). No sexual cycle or MAT locus has been described for S. schenckii, but it has been speculated that sexual reproduction may be extant in this fungal species on the basis of population genetic studies (191,196).…”

“…6). Further analysis revealed that the significantly larger MAT locus in Coccidioides species results from the capture of the flanking APN2 and COX13 genes, which now exhibit higher sequence divergence (70,189 .html]), a MAT1-2 HMG gene flanked by SLA2, APN2, and COX13 was identified by using Blastn and tBlastx searches (W. Li and J. Heitman, unpublished data). The orientation of these genes is the same as that of the most closely related species, H. capsulatum.…”