LaeA-Regulated Fungal Traits Mediate Bacterial Community Assembly

• Published in: mBio Vol. 14; no. 3; p. e0076923
• Main Authors: Tannous, Joanna, Cosetta, Casey M, Drott, Milton T, Rush, Tomás A, Abraham, Paul E, Giannone, Richard J, Keller, Nancy P, Wolfe, Benjamin E
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 27.06.2023; American Society for Microbiology (ASM)
• Subjects: Anti-Bacterial Agents - metabolism; Anti-Bacterial Agents - pharmacology; Bacteria - genetics; Base Sequence; BASIC BIOLOGICAL SCIENCES; Editor's Pick; Food Microbiology; fungal metabolites; Fungi - genetics; Fungi - metabolism; microbiome; Penicillium; Penicillium - genetics; Penicillium - metabolism; Research Article; fungal metabolites; Penicillium; microbiome
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mbio.00769-23

Potent antimicrobial metabolites are produced by filamentous fungi in pure culture, but their ecological functions in nature are often unknown. Using an antibacterial isolate and a cheese rind microbial community, we demonstrate that a fungal specialized metabolite can regulate the diversity of bacterial communities. Inactivation of the global regulator, LaeA, resulted in the loss of antibacterial activity in the isolate. Cheese rind bacterial communities assembled with the deletion strain had significantly higher bacterial abundances than the wild-type strain. RNA-sequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in the deletion strain. Inactivation of a core gene in the pseurotin biosynthetic cluster restored bacterial community composition, confirming the role of pseurotins in mediating bacterial community assembly. Our discovery demonstrates how global regulators of fungal transcription can control the assembly of bacterial communities and highlights an ecological role for a widespread class of fungal specialized metabolites. Cheese rinds are economically important microbial communities where fungi can impact food quality and aesthetics. The specific mechanisms by which fungi can regulate bacterial community assembly in cheeses, other fermented foods, and microbiomes in general are largely unknown. Our study highlights how specialized metabolites secreted by a species can mediate cheese rind development via differential inhibition of bacterial community members. Because LaeA regulates specialized metabolites and other ecologically relevant traits in a wide range of filamentous fungi, this global regulator may have similar impacts in other fungus-dominated microbiomes.