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Surfactin inhibits Fusarium graminearum by accumulating intracellular ROS and inducing apoptosis mechanisms

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Abstract

Fusarium graminearum, a devastating fungal pathogen, is the main pathogen of Fusarium head blight (FHB) in wheat globally; it results in significant yield loss and mycotoxin contamination that severely threatens global wheat production and food safety. However, despite ongoing efforts, controlling this pathogen still remains a major challenge. Surfactin, primarily synthesized by Bacillus sp. via non-ribosomal peptide synthetases, exhibits potent surfactant and antibacterial properties, but its antifungal mechanism has yet to be fully elucidated. We found that the EC50 of surfactin against hyphal growth of F. graminearum was 102.1 µg/mL, and control efficacy against wheat FHB under field conditions achieved 86.38% in wheat cultivar Huaimai 40 and 81.60% in wheat cultivar Zhoumai 36, indicating that surfactin has potential antifungal activity against F. graminearum. Accumulated intracellular ROS, decreased mitochondrial membrane potential (MMP), activated metacaspase activity and condensed chromatin, were induced by surfactin in F. graminearum hyphae, suggesting that growth inhibition of fungus is mainly caused by apoptosis-like cell death. Furthermore, accumulated intracellular ROS was evidenced to act as a key mediator of surfactin-induced apoptosis. Broad-spectrum caspase inhibitor Z-VAD-FMK treatment indicated that surfactin induces caspase-independent apoptosis in F. graminearum. Collectively, this study provides evidence that surfactin induces a ROS-mediated mitochondrial apoptosis in F. graminearum hyphae, and may exert its antifungal activity against F. graminearum by activating apoptosis. This study demonstrates the potential of surfactin as an antifungal agent for FHB biocontrol, provides a new perspective on the antifungal mechanism of surfactin against filamentous fungi, and contributes to the application of surfactin-producing microbes in the biocontrol of plant diseases.

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Data availability

The datasets generated during and/or analysed during this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This work was supported by National natural science foundation of China (32172280), Natural science foundation of Henan province (182300410042) and the earmarked fund for CARS-13.

Funding

This study was funded by National natural science foundation project of China (32172280), Natural science foundation of Henan province (182300410042) and the earmarked fund for CARS-13.

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Authors and Affiliations

  1. School of Biological Engineering, Henan University of Technology, Zhengzhou, 450001, China

    Chen Liang, Xu Xi-xi, Sun Yun-xiang, Xin Qiu-hua, Lv Yang-yong, Hu Yuan-sen & Bian Ke

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  1. Chen Liang
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  2. Xu Xi-xi
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  3. Sun Yun-xiang
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  4. Xin Qiu-hua
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  7. Bian Ke
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Contributions

CL: Investigation, Conceptualization, Data curation, Formal analysis, Methodology, Writing-original draft, Writing-review & editing, Supervision. XX: Data curation, Formal analysis, Methodology, Writing-original draft, Writing-review & editing. SY: Data curation, Formal analysis, Methodology. XQ: Data curation, Formal analysis, Methodology. LY: Investigation, Formal analysis, Methodology. HY: Resources, Supervision, Project administration. BK: Conceptualization, Resources, Supervision, Project administration.

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Correspondence to Chen Liang.

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Liang, C., Xi-xi, X., Yun-xiang, S. et al. Surfactin inhibits Fusarium graminearum by accumulating intracellular ROS and inducing apoptosis mechanisms. World J Microbiol Biotechnol 39, 340 (2023). https://doi.org/10.1007/s11274-023-03790-2

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