Unisexual Reproduction Enhances Fungal Competitiveness by Promoting Habitat Exploration via Hyphal Growth and Sporulation

Abstract

Unisexual reproduction is a novel homothallic sexual cycle recently discovered in both ascomycetous and basidiomycetous pathogenic fungi. It is a form of selfing that induces the yeast-to-hyphal dimorphic transition in isolates of the ␣ mating type of the human fungal pathogen Cryptococcus neoformans. Unisexual reproduction may benefit the pathogen by facilitating sexual reproduction in the absence of the opposite a mating type and by generating infectious propagules called basidiospores. Here, we report an independent potential selective advantage of unisexual reproduction beyond genetic exchange and recombination. We competed a wild-type strain capable of undergoing unisexual reproduction with mutants defective in this developmental pathway and found that unisexual reproduction provides a considerable dispersal advantage through hyphal growth and sporulation. Our results show that unisexual reproduction may serve to facilitate access to both nutrients and potential mating partners and may provide a means to maintain the capacity for dimorphic transitions in the environment. Sexual reproduction is pervasive and yet has established costs, including the time and energy devoted to locating a mate. A limited availability of mating partners of the opposite sex may further exacerbate this cost. The human fungal pathogen Cryptococcus neoformans illustrates this dilemma because its populations predominantly contain isolates of the ␣ mating type and few, if any, of the a mating type, restricting opportunities for conventional a-␣ opposite-sex mating (1, 2, 3). C. neoformans may overcome this barrier in part by undergoing unisexual reproduction-an alternative mode of sexual cycle involving cells of only one mating type, most commonly ␣ (4). Unisexual reproduction can confer benefits by generating adaptive genotypic diversity through recombination and by producing spore progeny that are readily dispersed aerially and inhaled as infectious propagules. Here, we report a novel way in which unisexual reproduction benefits C. neoformans, involving hyphal development to promote foraging and increased access to nutrients and facilitating the dispersal of spores.C. neoformans grows asexually as a budding yeast but differentiates into hyphae upon unisexual reproduction during solo culture of self-fertile isolates on appropriate growth media (4). Unisexual reproduction involves the formation of an extensive monokaryotic mycelium and terminal fruiting structures called basidia wherein meiosis occurs, and long chains of meiotic spores decorate the outer surface of the basidia (5). Components of a pheromone-responsive mitogen-activated protein kinase (MAPK) pathway are responsible for the yeast-to-hypha transition, and the absence of key elements, including the protein kinase Ste7 or the transcription factor Mat2, blocks unisexual reproduction and traps C. neoformans in the yeast form (6,7,8). While a functional MAPK pathway is necessary for morphological differentiation, the meiotic machinery, including Dmc1 and Spo11, is essential f...

From two to one: Unipolar sexual reproduction

“…Being capable of undergoing either homothallic or heterothallic sexual reproduction allows the organism to alleviate costs associated with mating, and to better survive and expand in hostile or changing environments by generating novel genotypes, increasing genetic diversity to facilitate natural selection, producing spores that are more resistant to harsh environments, as well as by transitioning into hyphal growth forms that are better at acquiring nutrients from the environment (Fu et al, 2014; Phadke et al, 2013). The frequent transitions between vegetative growth and mating, or between homothallic and heterothallic sexual reproduction, illustrate the balance between inbreeding and outcrossing, and are likely a response to specific environmental cues that the organism has evolved to recognize and respond to by undergoing one mode of reproduction or the other.…”

Unisexual versus bisexual mating in Cryptococcus neoformans: Consequences and biological impacts

“…These morphologically differentiated cell types provide plasticity for environmental adaptation. For example, C. neoformans can employ the hyphae produced by the unisexual cycle to explore the environment and forage for nutrients (Phadke et al, 2013), and spores can be easily dispersed widely by wind or water and are resistant to adverse environmental conditions (Alvarez and Casadevall, 2006; Botts et al, 2009). The exploration of the environment may also have other beneficial effects such as bringing mating ready cells into contact with distant mating partners, either through the production of hyphae to explore the local environment or the production of spores for wider dispersal.…”

The cryptic sexual strategies of human fungal pathogens

“…showed that unisexual mating in C. neoformans resulted in phenotypic variants, the majority of which were due to chromosome aneuploidies 40 . Same-sex mating can provide an additional selective advantage to C. neoformans as hyphal forms induced during mating allow for nutrient foraging over an increased area 47 .…”