Integrated Omics-Based Discovery of Novel Genes, Secondary Metabolites Clusters, and Small Molecules in Penicillium spp. with Disparate Fungal Isolates

Penicillium expansum is a ubiquitous postharvest pathogen of pome fruit that causes blue mold decay of apple fruit while another member of the genus, P. chrysogenum, is a well-studied saprophyte used for antibiotic and small molecule production. While these two fungi have been investigated individually, the recent discovery of P. chrysogenum hindering P. expansum apple fruit infection has not been well studied. To shed light on this interaction between the two species, we conducted a comparative transcriptomic, metabolomic, and genomic study. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for the P. chrysogenum isolates, and different between P. expansum isolates. Further, the two P. chrysogenum genomes revealed secondary metabolite gene clusters that differed from P. expansum. This included the absence of an intact patulin gene cluster in P. chrysogenum, which corroborates the metabolomic data regarding the species’ inability to produce patulin. Additionally, P. expansum virulence gene homologues were identified in P. chrysogenum and were similarly transcriptionally regulated in vitro. Molecules with potential antimicrobial activity, and phytohormones like indole-3-acetic acid (IAA), were detected for the first time in P. expansum while pharmacological compounds like the well-studied antibiotic penicillin G were identified in P. chrysogenum culture supernatants. Our findings provide new omics-based resources that enable the study of small molecule production of interest, the potential of Penicillium-derived antimicrobials for postharvest decay control, and P. expansum’s metabolites roles in host-pathogen interactions.