Antifungal mechanisms of volatile organic compounds and lactic acid produced by Lactiplantibacillus pentosus and their biocontrol application in fresh corn against Fusarium graminearum.

Abstract

Fusarium graminearum causes cereal spoilage and mycotoxin production. Currently, biocontrol microorganisms have emerged as a safe and promising strategy to manage the contamination of toxin-producing fungi in cereal grains. The primary objective was to elucidate the antifungal mechanism of an isolated strain of Lactiplantibacillus pentosus Q11 against F. graminearum and to evaluate the preservative effects of its cell-free supernatant (CFS) in fresh sweet corn. In vitro antifungal assays of L. pentosus Q11 showed strong antagonistic activity against F. graminearum, Aspergillus flavus, and Penicillium expansum, as well as the ability to reduce zearalenone. Moreover, whole-genome analysis revealed no genes related to virulence and antimicrobial resistance, and no hemolytic activity was observed, which suggested the potential safety of strain Q11. Moreover, the CFS of L. pentosus Q11 effectively inhibited the mycelial growth of F. graminearum, disrupted hyphal integrity, and induced fungal cell death. Moreover, 3 organic acids and 38 volatile compounds in the CFS of Q11 strain were identified by SPME-GC-MS and HPLC, in which 2-nonanone, 2-methylpyrazine, lactic acid, acetic acid were predominant compounds. The CFS and lactic acid combined with 2-nonanone severely damaged hyphae of F. graminearum, by disrupting cell membrane and wall, leading to leakage of intracellular substances, showing a synergistic antifungal effect of the two vital compounds. Subsequently, the treatments of CFS and combined agents significantly decreased 88.05% - 89.52% of fungal populations, and AFB1 and DON mycotoxin accumulation in fresh sweet corn after 12 days of storage compared to the control. The malondialdehyde content in the treated corn was decreased by 29.25% - 31.50%, consistent with the higher activities of POD and APX, thereby preserving their sensory attributes and nutritional quality. Metabolomic analysis revealed that L-glutamate, γ-glutamylcysteine, and oxidized glutathione were significantly downregulated in the glutathione metabolism pathway in the treated corn, indicating that CFS containing lactic acid and 2-nonanone could repress fungal growth and alleviate oxidative stress in fresh sweet corn. Overall, these findings demonstrate that L. pentosus Q11 with synergistic volatile organic compounds and lactic acid is a promising biocontrol agent in preserving fresh sweet corn.