Omics-Based Comparison of Fungal Virulence Genes, Biosynthetic Gene Clusters, and Small Molecules in Penicillium expansum and Penicillium chrysogenum

<i>Penicillium expansum</i> is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, <i>Penicillium chrysogenum</i>, is a well-studied saprophyte valued for antibiotic and small molecule production. While these two fungi have been investigated individually, a recent discovery revealed that <i>P. chrysogenum</i> can block <i>P. expansum-</i>mediated decay of apple fruit. To shed light on this observation, we conducted a comparative genomic, transcriptomic, and metabolomic study of two <i>P. chrysogenum</i> (404 and 413) and two <i>P. expansum</i> (Pe21 and R19) isolates. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for <i>P. chrysogenum</i> isolates, and different between <i>P. expansum</i> isolates. Further, the two <i>P. chrysogenum</i> genomes revealed secondary metabolite gene clusters that varied widely from <i>P. expansum</i>. This included the absence of an intact patulin gene cluster in <i>P. chrysogenum</i>, which corroborates the metabolomic data regarding its inability to produce patulin. Additionally, a core subset of <i>P. expansum</i> virulence gene homologues were identified in <i>P. chrysogenum</i> and were similarly transcriptionally regulated in vitro. Molecules with varying biological activities, and phytohormone-like compounds were detected for the first time in <i>P. expansum</i> while antibiotics like penicillin G and other biologically active molecules were discovered in <i>P. chrysogenum</i> culture supernatants. Our findings provide a solid omics-based foundation of small molecule production in these two fungal species with implications in postharvest context and expand the current knowledge of the <i>Penicillium</i>-derived chemical repertoire for broader fundamental and practical applications.