Unisexual reproduction promotes competition for mating partners in the global human fungal pathogenCryptococcus deneoformans
Authors: Fu Ci , Thielhelm Torin P. , Heitman Joseph 
Published: January 2019

Courtship is pivotal for successful mating. However, courtship is challenging for theCryptococcus neoformansspecies complex, comprised of opportunistic fungal pathogens, as the majority of isolates are α mating type. In the absence of mating partners of the opposite mating type,C. deneoformanscan undergo unisexual reproduction, during which a yeast-to-hyphal morphological transition occurs. Hyphal growth during unisexual reproduction is a quantitative trait, which reflects a strain’s ability to undergo unisexual reproduction. In this study, we determined whether unisexual reproduction confers an ecological benefit by promoting foraging for mating partners. Through competitive mating assays using strains with different abilities to produce hyphae, we showed that unisexual reproduction potential did not enhance competition for mating partners of the same mating type, but when cells of the opposite mating type were present, cells with enhanced hyphal growth were more competitive for mating partners of either the same or opposite mating type. Enhanced mating competition was also observed in a strain with increased hyphal production that lacks the mating repressor geneGPA3, which contributes to the pheromone response. Hyphal growth in unisexual strains also enables contact between adjacent colonies and enhances mating efficiency during mating confrontation assays. The pheromone response pathway activation positively correlated with unisexual reproduction hyphal growth during bisexual mating and exogenous pheromone promoted bisexual cell fusion. Despite the benefit in competing for mating partners, unisexual reproduction conferred a fitness cost. Taken together, these findings suggestC. deneoformansemploys hyphal growth to facilitate contact between colonies at long distances and utilizes pheromone sensing to enhance mating competition.

Author Summary

Sexual reproduction plays a pivotal role in shaping fungal population structure and diversity in nature. The global human fungal pathogenCryptococcus neoformansspecies complex evolved distinct sexual cycles: bisexual reproduction between mating partners of the opposite mating types, and unisexual reproduction with only one mating type. During both sexual cycles, cells undergo a yeast-to-hyphal morphological transition and nuclei diploidize through either cell-cell fusion followed by nuclear fusion during bisexual reproduction or endoreplication during unisexual reproduction. Despite the complex sexual life cycle, the majority of Cryptococcal isolates are α mating type. Albeit the scarcity ofMATacells in the environment, meiotic recombination is prevalent. To decipher this conundrum, we ask whether there is an underlying mechanism in whichCryptococcusspecies increase their mating opportunities. In this study, we showed that the undirected hyphal growth during unisexual reproduction enablesMATα cells to forage for mating partners over a larger surface area, and whenMATα hyphae come into close proximity of rareMATacells, pheromone response pathway activation in bothMATα andMATacells can further enhance mating. This mating enhancement could promote outcrossing and facilitate genome reshuffling via meiotic recombination.