Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus

Abstract

Aspergillus fumigatus is a saprotrophic fungus whose spores are ubiquitous in the atmosphere. It is also an opportunistic human pathogen in immunocompromised individuals, causing potentially lethal invasive infections, and is associated with severe asthma and sinusitis. The species is only known to reproduce by asexual means, but there has been accumulating evidence for recombination and gene flow from population genetic studies, genome analysis, the presence of mating-type genes and expression of sex-related genes in the fungus. Here we show that A. fumigatus possesses a fully functional sexual reproductive cycle that leads to the production of cleistothecia and ascospores, and the teleomorph Neosartorya fumigata is described. The species has a heterothallic breeding system; isolates of complementary mating types are required for sex to occur. We demonstrate increased genotypic variation resulting from recombination between mating type and DNA fingerprint markers in ascospore progeny from an Irish environmental subpopulation. The ability of A. fumigatus to engage in sexual reproduction is highly significant in understanding the biology and evolution of the species. The presence of a sexual cycle provides an invaluable tool for classical genetic analyses and will facilitate research into the genetic basis of pathogenicity and fungicide resistance in A. fumigatus, with the aim of improving methods for the control of aspergillosis. These results also yield insights into the potential for sexual reproduction in other supposedly 'asexual' fungi.

Mating type markers reveal high levels of heterothallism in Leptographium sensu lato

“…It is plausible that their sexual states have not been seen due to their heterothallic nature and the fact that they have been collected in the absence of an opposite mating strain. This is similar to the situation for various other fungi, thought to be asexual but later shown to be heterothallic and where sexual states have recently been discovered for some of the species (Horn et al, 2009;O'Gorman et al, 2008;Seidl et al, 2009). Duong et al (2012) were able to show that G. alacris is heterothallic by randomly crossing different isolates in all possible combinations.…”

Large and variable genome size unrelated to serpentine adaptation but supportive of cryptic sexuality in Cenococcum geophilum

“…A sexual stage in C. geophilum was also recently proposed by Spatafora et al (2012) based on the large genetic diversity detected in this species and a close phylogenetic relationship with Glonium, for which a sexual stage has been identified. As sexual reproduction in fungi can be geographically isolated and therefore difficult to detect (O'Gorman et al 2009;Spatafora et al 2012), it is not surprising that we found only 6 in 40 isolates to deviate from a presumed haploid condition. However, the existence of a parasexual cycle is not the only possible explanation for the observed variance in ploidy level.…”

Sexual reproduction and mating-type–mediated strain development in the penicillin-producing fungus Penicillium chrysogenum

“…These strains were either wild type (from different geographic origins) or production strains with high penicillin titers (Table S1). Various combinations of growth media and pairings were tested, including the use of conditions recently shown to induce sexual reproduction in Aspergillus fumigatus and related aspergilli (18,20). When crosses were performed on different oatmeal agars in sealed Petri dishes in the dark at 15-27°C, cleistothecia [sexual reproductive structures characteristic of Penicillium species and some other ascomycete fungi (18,21)] were formed in most but not all crosses in the contact zone of the two mating partners after incubation from 5 wk to 3 mo, but these were sterile with no ascospores produced.…”