The emblematic fungus Penicillium roqueforti is used throughout the world as a starter culture in the production of blue-veined cheeses. Like other industrial filamentous fungi, P. roqueforti was thought to lack a sexual cycle. However, an ability to induce recombination is of great economic and fundamental importance, as it would make it possible to transform and improve industrial strains, promoting the creation of novel phenotypes and eliminating the deleterious mutations that accumulate during clonal propagation. We report here, for the first time, the induction of the sexual structures of P. roqueforti — ascogonia, cleistothecia and ascospores. The progeny of the sexual cycle displayed clear evidence of recombination. We also used the recently published genome sequence for this species to develop microsatellite markers for investigating the footprints of recombination and population structure in a large collection of isolates from around the world and from different environments. Indeed, P. roqueforti also occurs in silage, wood and human-related environments other than cheese. We found tremendous genetic diversity within P. roqueforti, even within cheese strains and identified six highly differentiated clusters that probably predate the use of this species for cheese production. Screening for phenotypic and metabolic differences between these populations could guide future development strategies.
Fungi exhibit substantial morphological and genetic diversity, often associated with cryptic species differing in ecological niches. Penicillium roqueforti is used as a starter culture for blue-veined cheeses, being responsible for their flavor and color, but is also a common spoilage organism in various foods. Different types of blue-veined cheeses are manufactured and consumed worldwide, displaying specific organoleptic properties. These features may be due to the different manufacturing methods and/or to the specific P. roqueforti strains used. Substantial morphological diversity exists within P. roqueforti and, although not taxonomically valid, several technological names have been used for strains on different cheeses (e.g., P. gorgonzolae, P. stilton). A worldwide P. roqueforti collection from 120 individual blue-veined cheeses and 21 other substrates was analyzed here to determine (i) whether P. roqueforti is a complex of cryptic species, by applying the Genealogical Concordance Phylogenetic Species Recognition criterion (GC-PSR), (ii) whether the population structure assessed using microsatellite markers correspond to blue cheese types, and (iii) whether the genetic clusters display different morphologies. GC-PSR multi-locus sequence analyses showed no evidence of cryptic species. The population structure analysis using microsatellites revealed the existence of highly differentiated populations, corresponding to blue cheese types and with contrasted morphologies. This suggests that the population structure has been shaped by different cheese-making processes or that different populations were recruited for different cheese types. Cheese-making fungi thus constitute good models for studying fungal diversification under recent selection.
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