Omics-based comparison of fungal virulence genes, biosynthetic gene clusters, and small molecules in penicillium expansum and penicillium chrysogenum

Authors: Bartholomew, Holly; Gottschalk, Christopher; Cooper, Bret; Bukowski, Michael; Yang, Ronghui; Gaskins, Verneta; LUCIANO-ROSARIO, DIANIRIS - Orise Fellow; Fonseca, Jorge; Jurick Ii, Wayne

Submitted to: The Journal of Fungi
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/25/2024
Publication Date: 12/28/2024
Citation: Bartholomew, H.P., Gottschalk, C.C., Cooper, B., Bukowski, M.R., Yang, R., Gaskins, V.L., Luciano-Rosario, D., Fonseca, J.M., Jurick Ii, W.M. 2024. Omics-based comparison of fungal virulence genes, biosynthetic gene clusters, and small molecules in penicillium expansum and penicillium chrysogenum. The Journal of Fungi. 11(1). Article e14. https://doi.org/10.3390/jof11010014.
DOI: https://doi.org/10.3390/jof11010014

Interpretive Summary: Blue mold decay, caused by the fungus Penicillium expansum, is commonly found in stored pome fruit and contributes to reduced product quality that results in food waste and loss. Patulin, a major mycotoxin produced by P. expansum, is harmful to human and animal health, and has antifungal activity. As conventional methods of decay control (e.g. fungicides) are being reduced, alternatives are being sought to reduce food waste from mycotoxin-producing fungi. The current efforts strive to compare two non-pathogenic Penicillium chrysogenum isolates to two virulent P. expansum isolates in order to better characterize genes and compounds involved in apple decay, and for potential biocontrol development. We demonstrate species-level genetic and metabolomic differences, such as the inability of P. chrysogenum to produce patulin. Further, many P. expansum metabolites produced suggest the fungus may be able to alter the apple host. The P. chrysogenum isolates produced many potential pharmacological and antimicrobial compounds, including the antibiotic penicillin, that may be harnessed by industry for therapeutics or even new fungicide treatment options. Through these discoveries, improvements can be made to maintain fruit quality during storage and simultaneously reduce mycotoxin contamination.

Technical Abstract: Penicillium expansum is a ubiquitous pathogenic fungus that causes blue mold decay of apple fruit postharvest, and another member of the genus, P. chrysogenum, 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 P. chrysogenum can block P. expansum-mediated decay of apple fruit. To shed light on this observation, we conducted a comparative genomic, transcriptomic, and metabolomic study of two P. chrysogenum (404 and 413) and two P. expansum (Pe21 and R19) isolates. Global transcriptional and metabolomic outputs were disparate between the species, nearly identical for P. chrysogenum isolates, and different between P. expansum isolates. Further, the two P. chrysogenum genomes revealed secondary metabolite gene clusters that varied widely 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, a core subset of P. expansum virulence gene homologues were identified in P. chrysogenum and were similarly transcriptionally regulated in vitro. Molecules with varying biological activities, and phytohormone-like compounds were detected for the first time in P. expansum while antibiotics like penicillin G and other biologically active molecules were discovered in P. chrysogenum 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 Penicillium-derived chemical repertoire for broader fundamental and practical applications.