Biocontrol mechanism of a newly isolated Streptomyces sp. JL2001 against Ralstonia solanacearum via aerugine

Abstract

Bacterial wilt, caused by the soil-borne phytopathogen Ralstonia solanacearum (R. solanacearum), poses a serious threat to global agriculture. In this study, 26 actinomycete strains were isolated from the rhizosphere of traditional Chinese medicinal plants. Among them, Streptomyces sp. JL2001 exhibited strong inhibitory activity against R. solanacearum both in vitro and in planta. UPLC-QTOF-MS/MS analysis identified aerugine as the major active compound, alongside five structurally related 2-hydroxyphenylthiazoline derivatives. Chemically synthesized aerugine showed broad-spectrum antibacterial activity, significantly inhibiting planktonic growth and biofilm formation and alleviating bacterial wilt symptoms in tomato seedlings under hydroponic and soil-based conditions. Mechanistically, aerugine disrupts bacterial membranes, interferes with lipid metabolism, and downregulates key virulence systems, including flagellar assembly and the type III secretion system. These findings were supported by electron microscopy, proteomic profiling, and qPCR validation. Whole-genome sequencing of JL2001 revealed a 7.75 Mb chromosome containing 22 biosynthetic gene clusters (BGCs), including a thiazostatin-like NRPS-dependent BGC likely responsible for aerugine biosynthesis. Importantly, soil-based assays demonstrated that aerugine significantly and dose-dependently suppressed R. solanacearum in natural soil, while also inducing changes in microbial composition. Later-stage increases in bacterial abundance and diversity, particularly of morphologically distinct non-pathogenic colonies, suggest that aerugine not only eliminates pathogens but may also promote beneficial microbiota -a dual protection mechanism. This study highlights Streptomyces sp. JL2001 and aerugine as promising agents for the sustainable control of bacterial wilt and provides new insights into their molecular antibacterial mechanisms.

Keywords: Aerugine; Biocontrol; Biosynthetic gene clusters (BGCs); R. solanacearum; Rhizosphere streptomycetes; Streptomyces sp. JL2001.