Speciation despite globally overlapping distributions in Penicillium chrysogenum: the population genetics of Alexander Fleming’s lucky fungus

Abstract

Eighty years ago, Alexander Fleming described the antibiotic effects of a fungus that had contaminated his bacterial culture, kick starting the antimicrobial revolution. The fungus was later ascribed to a putatively globally distributed asexual species, Penicillium chrysogenum. Recently, the species has been shown to be genetically diverse, and possess mating-type genes. Here, phylogenetic and population genetic analyses show that this apparently ubiquitous fungus is actually composed of at least two genetically distinct species with only slight differences detected in physiology. We found each species in air and dust samples collected in and around St Mary's Hospital where Fleming worked. Genotyping of 30 markers across the genome showed that preserved fungal material from Fleming's laboratory was nearly identical to derived strains currently in culture collections and in the same distinct species as a wild progenitor strain of current penicillin producing industrial strains rather than the type species P. chrysogenum. Global samples of the two most common species were found to possess mating-type genes in a near 1:1 ratio, and show evidence of recombination with little geographic population subdivision evident. However, no hybridization was detected between the species despite an estimated time of divergence of less than 1MYA. Growth studies showed significant interspecific inhibition by P. chrysogenum of the other common species, suggesting that competition may facilitate species maintenance despite globally overlapping distributions. Results highlight under-recognized diversity even among the best-known fungal groups and the potential for speciation despite overlapping distribution.

Presence and Functionality of Mating Type Genes in the Supposedly Asexual Filamentous Fungus Aspergillus oryzae

“…It is noteworthy that the tane-koji starter cultures sold to brewing companies usually consist of strains that are mixed beforehand, and it is therefore possible that strains of opposite mating types might meet under industrial growth conditions. There have been similar reports of the presence of both MAT1-1 and MAT1-2 isolates in populations of other "asexual" pezizomycete fungi, including Alternaria species (2), Aspergillus species (49,58), Rhynchosporium species (37,66), Cercospora species (21), Coccidioides species (18,40), and Penicillium chrysogenum (23,24). The only exception has been the asexual species Acremonium chrysogenum, used to produce cephalosporin, for which only the MAT1-1 genotype could be found in a preliminary survey (55).…”

Emerging fungal threats to animal, plant and ecosystem health

“…This ability of fungi to disperse results in some species with cosmopolitan distributions 5,49,50 . However, these species are in the minority and it is noticeable that few fungi exhibit truly globally distributions; instead they exhibit spatially restricted endemic ranges 51 .…”

Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen

“…Few researchers, however, have examined the utility of these methods for closely related asexual taxa that are morphologically indistinguishable [22]. Phylogenetic analyses of closely-related taxa, such as rice [21], Drosophila [23], and cryptic fungal species, such as Penicillium [22,24], are at the intersection of population genetics and phylogenetics where the effects of coalescent stochasticity results in high levels of gene tree incongruence [17,25-27]. Estimating species trees for these taxa can be problematic; these methods could prove to be useful for closely-related asexual fungal taxa.…”