Antimicrobial mechanisms and secondary metabolite profiles of Streptomyces hygroscopicus subsp. hygroscopicus 5-4 against banana fusarium wilt disease using metabolomics

Tianyan Yun; Tao Jing; Xiaoping Zang; Dengbo Zhou; Kai Li; Yankun Zhao; Wei Wang; Jianghui Xie

doi:10.3389/fmicb.2023.1159534

Antimicrobial mechanisms and secondary metabolite profiles of Streptomyces hygroscopicus subsp. hygroscopicus 5-4 against banana fusarium wilt disease using metabolomics

Front Microbiol. 2023 Jun 9:14:1159534. doi: 10.3389/fmicb.2023.1159534. eCollection 2023.

Authors

Tianyan Yun^#^{1

2}, Tao Jing^#^{1

2}, Xiaoping Zang^{1

2}, Dengbo Zhou¹, Kai Li¹, Yankun Zhao¹, Wei Wang¹, Jianghui Xie¹

Affiliations

¹ National Key Laboratory for Tropical Crop Breeding, Hainan Institute for Tropical Agricultural Resources, Chinese Academy of Tropical Agricultural Sciences (CATAS), Haikou, China.
² Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences (CATAS), Haikou, China.

^# Contributed equally.

Abstract

Fusarium wilt of bananas (FWB) is seriously affecting the sustainable development of the banana industry and is caused by the devastating soil-borne fungus Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4). Biological control is a promising strategy for controlling Fusarium wilt in bananas. We previously identified Streptomyces hygroscopicus subsp. hygroscopicus 5-4 with strong antifungal activity against the FWB. The most possible antimicrobial mechanism of strain 5-4 was explored using the metabolomics approach, light microscopy imaging, and transmission electron microscopy (TEM). The membrane integrity and ultrastructure of Foc TR4 was damaged after extract treatment, which was supported by the degradation of mycelium, soluble protein content, extracellular reducing sugar content, NADH oxidase activity, malondialdehyde content, mitochondrial membrane potential, and mitochondrial respiratory chain complex enzyme activity. The extracts of strain 5-4 cultivated at different times were characterized by a liquid chromatography-mass spectrometer (LC-MS). 647 known metabolites were detected in the extracts of strains 5-4. Hygromycin B, gluten exorphin B4, torvoside G, (z)-8-tetradecenal, piperitoside, sarmentosin, pubescenol, and other compounds were the main differential metabolites on fermentation culture for 7 days. Compared with strain 5-4 extracts, hygromycin B inhibited the mycelial growth of Foc TR4, and the EC₅₀ concentration was 7.4 μg/mL. These results showed that strain 5-4 could destroy the cell membrane of Foc TR4 to inhibit the mycelial growth, and hygromycin B may be the key antimicrobial active metabolite. Streptomyces hygroscopicus subsp. hygroscopicus 5-4 might be a promising candidate strain to control the FWB and provide a scientific basis for the practical application of hygromycin B as a biological control agent.

Keywords: Streptomyces hygroscopicus subsp. hygroscopicus; antifungal mechanism; fusarium wilt of banana; hygromycin B; metabolomics.

Grants and funding

This study has been supported by the China Agriculture Research System of MOF and MARA (CARS-31), the Natural Science Foundation of Hainan (322RC795 and 321QN0913), and the Central Public-Interest Scientific Institution Basal Research Fund for the Chinese Academy of Tropical Agricultural Sciences (No. 1630092022002).