Evolution of eukaryotic microbial pathogens via covert sexual reproduction

Abstract

Sexual reproduction enables eukaryotic organisms to reassort genetic diversity and purge deleterious mutations, producing better-fit progeny. Sex arose early and pervades eukaryotes. Fungal and parasite pathogens once thought asexual have maintained cryptic sexual cycles, including unisexual or parasexual reproduction. As pathogens become niche and host adapted, sex appears to specialize to promote inbreeding and clonality yet maintain outcrossing potential. During self-fertile sexual modes, sex itself may generate genetic diversity de novo. Mating-type loci govern fungal sexual identity; how parasites establish sexual identity is unknown. Comparing and contrasting fungal and parasite sex promises to reveal how microbial pathogens evolved and are evolving.

Figure 1

Sex and virulence of fungal pathogens. Four major human and plant fungal pathogens are illustrated to compare and contrast features of sexual reproduction and links to virulence.

Figure 2

MAT encoded cell identity determinants in pathogenic and model fungi. Genes resident within fungal MAT loci are illustrated for three phyla of the fungal kingdom. These genes encode transcription factors (homeodomain, HMG, α-domain) or pheromones or pheromone receptors that establish cell type identity, orchestrate sexual reproduction, and in some cases are linked to virulence.

Figure 3

Unisexual reproduction of pathogenic fungi. The opposite and same-sex cycles for C. neoformans and C. albicans are depicted. These reproductive cycles involve meiosis in C. neoformans but are currently thought to be parasexual in C. albicans. These alternative sexual cycles contribute to generate and maintain population diversity and same-sex mating likely also contributes to features of clonality observed for both of these common fungal pathogens.

Figure 4

On how Plasmodium gamete sexual identity may be specified. Three models are presented for how gamete identity might be specified in Plasmodium. These models are speculative and the intent is to suggest ways in which a single clonal isolate of Plasmodium might be capable of producing male or female gametocytes, based on precedents for other regulated switches in bacteria and fungi.