Fungal membrane determinants affecting sensitivity to antifungal cyclic lipopeptides from Bacillus spp

• Published in: Fungal biology 2024-11, Vol.128 (7), p.2080-2088
• Main Authors: Bakker, Charlotte, Graham, Hailey R., Popescu, Irina, Li, Melody, McMullin, David R., Avis, Tyler J.
• Format: Article
• Language: English
• Subjects: Antifungal Agents - metabolism; Antifungal Agents - pharmacology; Antifungal tolerance; Bacillus - chemistry; Bacillus - drug effects; Bacillus - metabolism; Cell Membrane - chemistry; Cell Membrane - drug effects; Cell Membrane - metabolism; Ergosterol - metabolism; Fengycin; Fungi - drug effects; Iturin; Lipopeptides - metabolism; Lipopeptides - pharmacology; Microbial Sensitivity Tests; Peptides, Cyclic - metabolism; Peptides, Cyclic - pharmacology; Plant pathogenic fungi; Surfactin
• ISSN: 1878-6146
• DOI: 10.1016/j.funbio.2024.08.006

Bacillus spp. produce numerous antimicrobial metabolites. Among these metabolites, cyclic lipopeptides (CLP) including fengycins, iturins, and surfactins are known to have varying antifungal activity against phytopathogenic fungi. The differential activities of CLP have been attributed to diverse mechanisms of action on fungal membranes. However, the precise biochemical determinants driving their antifungal modes of action have not been conclusively identified. In this study, three plant pathogenic fungi of varying lipopeptide sensitivities, Alternaria solani, Cladosporium cucumerinum, and Fusarium sambucinum, were studied to determine how their cell membrane lipid compositions may confer sensitivity and/or tolerance to fengycin, iturin, and surfactin. Results indicated that sensitivity to all three lipopeptides correlated with lower ergosterol content and elevated phospholipid fatty acid unsaturation. Fungal sensitivity to surfactin was also notably different than fengycin and iturin, as surfactin was influenced more by lower phosphatidylethanolamine amounts, higher levels of phosphatidylinositol, and less by phospholipid fatty acyl chain length. Results from this study provide insight into the fungal membrane composition of A. solani, F. sambucinum, and C. cucumerinum and the specific membrane characteristics influencing the antifungal effectiveness of fengycin, iturin, and surfactin. Understanding of these determinants should enable more accurate prediction of sensitivity-tolerance outcomes for other fungal species exposed to these important CLP. •Fungi were differentially sensitive to Bacillus lipopeptides.•Lipopeptide sensitivity correlated with ergosterol content.•Phospholipid fatty acid unsaturation and chain length were sensitivity determinants.•Surfactin sensitivity was different and influenced by phospholipid polar headgroups.