Bacterial-fungal crosstalk is defined by a fungal lactone mycotoxin and its degradation by a bacterial lactonase

• Published in: Applied and environmental microbiology 2024-06, Vol.90 (6), p.e0029924
• Main Authors: Dor, Shlomit, Nudel, Keren, Eagan, Justin L, Cohen, Rami, Hull, Christina M, Keller, Nancy P, Prusky, Dov, Afriat-Jurnou, Livnat
• Format: Article
• Language: English
• Subjects: Apples; Bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Biocompatibility; Biodegradation; Carboxylic Ester Hydrolases - genetics; Carboxylic Ester Hydrolases - metabolism; Degradation; Erwinia; Erwinia amylovora - drug effects; Erwinia amylovora - enzymology; Erwinia amylovora - genetics; Erwinia amylovora - metabolism; Fruit trees; Fungi; Gene expression; Lactones; Lactones - metabolism; Lactones - pharmacology; Malus - microbiology; Microbial Interactions; Microbiomes; Mycobacteriology; Mycotoxins; Pathogenicity; Pathogens; Patulin; Patulin - metabolism; Penicillium - enzymology; Penicillium - genetics; Penicillium - metabolism; Plant Diseases - microbiology; Population density; Quorum Sensing; Substrates
• ISSN: 0099-2240; 1098-5336; 1098-5336
• DOI: 10.1128/aem.00299-24

Bacteria, fungi, and mammals contain lactonases that can degrade the Gram-negative bacterial quorum sensing (QS) molecules N-acyl homoserine lactones (AHLs). AHLs are critical for bacteria to coordinate gene expression and pathogenicity with population density. However, AHL-degrading lactonases present variable substrate ranges, including degradation of the lactone mycotoxin patulin. We selected spp. as our model bacteria to further investigate this interaction. We find both native apple microbiome spp. and the fruit tree pathogen to be inhibited by patulin. At patulin concentrations that inhibited growth, expression of lactonase encoded by was increased. EaAiiA demonstrated the ability to degrade patulin as well, as where it reduced apple disease and patulin production by . Fungal-bacterial co-cultures revealed that the Δ strain failed to protect apples from infections, which contained significant amounts of patulin. Our results suggest that bacterial lactonase production can modulate the pathogenicity of in response to the secretion of toxic patulin. Chemical signaling in the microbial world facilitates the regulation of gene expression as a function of cell population density. This is especially true for the Gram-negative bacterial signal N-acyl homoserine lactone (AHL). Lactonases that deactivate AHLs have attracted a lot of attention because of their antibacterial potential. However, the involvement of these enzymes in inhibiting fungal pathogens and the potential role of these enzymes in bacterial-fungal interactions are unknown. Here, we find that a bacterial enzyme involved in the degradation of AHLs is also induced by and degrades the fungal lactone mycotoxin, patulin. This work supports the potential use of bacterial enzymes and/or the producing bacteria in controlling the post-harvest fruit disease caused by the patulin-producing fungus .