Discovery of niphimycin C from Streptomyces yongxingensis sp. nov. as a promising arochemical fungicide for controlling banana fusarium wilt by destroying the mitochondrial structure and function

Authors: CHEN, YUFENG - Chinese Academy Of Tropical Agricultural Sciences; WEI, YONGZAN - Chinese Academy Of Tropical Agricultural Sciences; CAI, BINGYU - Chinese Academy Of Tropical Agricultural Sciences; ZHOU, DENGBO - Chinese Academy Of Tropical Agricultural Sciences; QI, DENGFENG - Chinese Academy Of Tropical Agricultural Sciences; ZHANG, MIAOYI - Chinese Academy Of Tropical Agricultural Sciences; ZHAO, YANKUN - Chinese Academy Of Tropical Agricultural Sciences; LI, KAI - Chinese Academy Of Tropical Agricultural Sciences; Wedge, David; Pan, Zhiqiang - Peter; XIE, JIANGHUI - Chinese Academy Of Tropical Agricultural Sciences; WANG, WEI - Chinese Academy Of Tropical Agricultural Sciences

Submitted to: Journal of Agricultural and Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/12/2022
Publication Date: 9/28/2022
Citation: Chen, Y., Wei, Y., Cai, B., Zhou, D., Qi, D., Zhang, M., Zhao, Y., Li, K., Wedge, D.E., Pan, Z., Xie, J., Wang, W. 2022. Discovery of niphimycin C from Streptomyces yongxingensis sp. nov. as a promising arochemical fungicide for controlling banana fusarium wilt by destroying the mitochondrial structure and function. Journal of Agricultural and Food Chemistry. https://doi.org/10.1021/acs.jafc.2c02810.
DOI: https://doi.org/10.1021/acs.jafc.2c02810

Interpretive Summary: Fusarium wilt of banana, the disease caused by Fusarium oxysporum (Foc), is common and the most destructive soil-borne fungal disease in the banana industry. To search for tools to control this disease, a Streptomyces strain was isolated from a soft coral that exhibits the inhibition of Foc mycelial growth up to 75%. A compound, malolactomycin C, showing significant antifungal activity, was then isolated from this strain. It inhibits the mycelial growth and spore germination of Foc with a 1.26 µg/mL of EC50 value. The disease symptom was significantly reduced in pot experiments with disease index decreased by 60.47% compared to the control. Furthermore, it also has a range of antifungal activities against selected fungal strains. These results suggest that this compound could be developed as an effective agrochemical fungicide for controlling the fusarium wilt.

Technical Abstract: Banana Fusarium wilt caused by Fusarium oxysporum f. sp. cubense (Foc) is the most destructive soil-borne fungal disease. Foc tropical race 4 (Foc TR4) can infect nearly all banana varieties. The excessive use of synthetic fungicides leads to environmental pollution and human health hazards. Natural antifungal agents are considered as an alternative to fungicides. Here, we report that a novel strain was isolated from a marine soft coral, which was identified as Streptomyces yongxingensis sp. nov. (JCM 34965). Malolactomycin C, a compound isolated from this strain, inhibits the mycelial growth and spore germination of Foc TR4 with a 1.26 µg/mL of EC50 value. The compound caused the functional loss of mitochondria and the disorder of metabolism of Foc TR4 cells. Further study showed that malolactomycin C reduced key enzyme activities of the tricarboxylic acid (TCA) cycle and the electron transport chain (ETC). Its broad-spectrum antifungal activity against the selected 12 phytopathogenic fungi supported the above antifungal mechanism. In a pot experiment, the disease indexes of banana plantlets treated with malolactomycin C were decreased and the infection of Foc TR4 in roots was inhibited. These results suggest that malolactomycin C could be a potential agrochemical fungicide for the management of the fungal disease.