Frequent transitions in mating- type locus chromosomal organization in Malassezia and early steps in sexual reproduction

Fungi in the basidiomycete genus Malassezia are the most prevalent eukaryotic microbes resident on the skin of human and other warm-blooded animals and have been implicated in skin diseases and systemic disorders. Analysis of Malassezia genomes revealed that key adaptations to the skin microenvironment have a direct genomic basis, and the identification of mating/meiotic genes suggests a capacity to reproduce sexually, even though no sexual cycle has yet been observed. In contrast to other bipolar or tetrapolar basidiomycetes that have either two linked mating- type-determining (MAT) loci or two MATloci on separate chromosomes, in Malassezia species studied thus far the two MATloci are arranged in a pseudobipolar configuration (linked on the same chromosome but capable of recombining). By generating additional chromosome level genome assemblies, and an improved Malassezia phylogeny, we infer that the pseudo bipolar arrangement was the ancestral state of this group and revealed six independent transitions to tetrapolarity, seemingly driven by centromere fission or translocations in centromere-flanking regions. Additionally, in an approach to uncover a sexual cycle, Malassezia furfur strains were engineered to express different MAT alleles in the same cell. The resulting strains produce hyphae reminiscent of early steps in sexual development and display upregulation of genes associated with sexual development as well as others encoding lipases and a protease potentially relevant for pathogenesis of the fungus. Our study reveals a previously unseen genomic relocation of mating type loci in fungi and provides insight toward the identification of a sexual cycle in Malassezia, with possible implications for pathogenicity.

Automated summary

Fungi in the genus Malassezia, which are commonly found on the skin of humans and other warm-blooded animals, have been linked to skin diseases and systemic disorders. Analysis of Malassezia genomes suggests that their ability to adapt to the skin microenvironment is directly influenced by their genetic makeup. Despite the absence of observed sexual reproduction, the presence of mating/meiotic genes suggests a potential for sexual reproduction in Malassezia. The arrangement of mating type loci in Malassezia has been found to be different from other basidiomycetes, indicating an ancestral state of the genus.