LaeA-regulated fungal traits mediate bacterial community assembly

Authors: TANNOUS, JOANNA - Tufts University; COSETTA, CASEY - Tufts University; Drott, Milton; RUSH, TOMAS - University Of Wisconsin; ABRAHAM, PAUL - University Of Wisconsin; GIANNONE, RICHARD - University Of Wisconsin; KELLER, NANCY - University Of Wisconsin; WOLFE, BENJAMIN - Tufts University

Submitted to: mBio
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/3/2023
Publication Date: 5/9/2023
Citation: Tannous, J., Cosetta, C.M., Drott, M.T., Rush, T.A., Abraham, P.E., Giannone, R.J., Keller, N.P., Wolfe, B.E. 2023. LaeA-regulated fungal traits mediate bacterial community assembly. mBio. 14(3). Article e00769-23. https://doi.org/10.1128/mbio.00769-23.
DOI: https://doi.org/10.1128/mbio.00769-23

Interpretive Summary: Storage of cheese in caves is an extremely important way in which dairy can be stored for long periods of time. As such, the federal government has invested substantially in cheese making and cheese storage. During this storage process, a community of fungi and bacterial form on the outside of cheeses forming rinds. It has become increasingly clear that the organisms present in the rind can have huge impacts on the long-term stability of cheese in storage conditions. In particular, some microbes seem to be able to disturb a stable community and eventually cause spoilage of cheeses. Here we demonstrate that the production of a specific compound, pseurotin, by a common cheese-associated fungus is fundamental in determining the ultimate microbial composition of cheese rinds. This result suggests that this fungus may be an important player in developing spoilage-resistant rinds on cheese and points to new opportunity to mitigate losses of this important agricultural product.

Technical Abstract: Potent antimicrobial metabolites are produced by filamentous fungi in pure culture, but their ecological functions in nature are often unknown. Using an antibacterial Penicillium 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 Penicillium isolate. Cheese rind bacterial communities assembled with the laeA deletion strain had significantly higher bacterial abundances than the wild-type strain. RNAsequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in the laeA 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.