Abstract
Cryptococcus neoformans is a ubiquitous human fungal pathogen that causes meningoencephalitis in predominantly immunocompromised hosts. The fungus is typically haploid, and sexual reproduction involves two individuals with opposite mating types/sexes, α and a. However, the overwhelming predominance of mating type (MAT) α over a in C. neoformans populations limits α–a mating in nature. Recently it was discovered that C. neoformans can undergo same-sex mating under laboratory conditions, especially between α isolates. Whether same-sex mating occurs in nature and contributes to the current population structure was unknown. In this study, natural αADα hybrids that arose by fusion between two α cells of different serotypes (A and D) were identified and characterized, providing definitive evidence that same-sex mating occurs naturally. A novel truncated allele of the mating-type-specific cell identity determinant SXI1α was also identified as a genetic factor likely involved in this process. In addition, laboratory-constructed αADα strains exhibited hybrid vigor both in vitro and in vivo, providing a plausible explanation for their relative abundance in nature despite the fact that AD hybrids are inefficient in meiosis/sporulation and are trapped in the diploid state. These findings provide insights on the origins, genetic mechanisms, and fitness impact of unisexual hybridization in the Cryptococcus population.
Highlights
The level of genetic variation within a species is correlated with evolutionary potential [1]
This fungus has two mating types/sexes, a and a, and mating typically requires two individuals with opposite mating types. It is mysterious why the a mating type is overwhelmingly predominant in nature and how the capacity for sexual reproduction is maintained in a largely unisexual population
We postulated that same-sex mating between a isolates may occur naturally, as it does under laboratory conditions
Summary
The level of genetic variation within a species is correlated with evolutionary potential [1]. Trypanosoma cruzi, the cause of Chagas disease, descends from two ancestral hybridization events [9,10]; influenza viruses undergo antigenic variations and host range shifts through hybridization and reassortment [11]; and in the parasite Leishmania, which has no known sexual cycle and a largely clonal population structure, recombinant strains can be generated through interspecific hybridization [12,13,14,15] Because of their morphological and genomic plasticity, fungi are subject to profound genetic changes, including those resulting from hybridization. Less is known about the impact of hybridization on the virulence of human pathogenic fungi
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