A novel quorum quencher, Rhodococcus pyridinivorans XN-36, is a powerful agent for the biocontrol of soft rot disease in various host plants

Abstract

Quorum sensing (QS) is a microbial cell–cell communication mechanism that regulates the virulence factor production in numerous pathogens, which plays a key role in microbial infections. QS-mediated microbial infections can be blocked via quorum quenching (QQ), which disrupts QS either by degradation of QS signals or interference of signal generation or perception. The pathogenicity of various diseases, including Pectobacterium carotovorum, is regulated by N-acyl homoserine lactone (AHL), a widely conserved QS signaling molecule. P. carotovorum can induce soft rot in a variety of crops and cause great economic losses to agricultural production. In this study, a newly isolated bacterium of Rhodococcus pyridinivorans XN-36 was identified as a novel QQ strain that can effectively degrade AHL and reduce the disease severity of P. carotovorum in host plants. Strain XN-36 was capable of rapidly degrading AHL without a lag phase, and over 85% of AHL (0.5 mmol·L−1) was degraded within 96 h. The metabolic intermediates of AHL biodegradation were detected and identified by gas chromatography-mass spectrometry (GC–MS) as lactamide and propenamide. Based on the chemical structure of AHL and intermediate metabolites, a novel metabolic pathway of AHL in strain XN-36 was proposed, which suggests that AHL could be degraded first by cleavage of its amide bond, followed by hydrolysis of the lactonic ring and subsequent metabolism. In addition, strain XN-36 participated in efficient degradation of a wide range of AHL signaling molecules including N-(3-oxohexanoyl)-L-homoserine lactone (OHHL), N-hexanoyl-L-homoserine lactone (C6HSL), N-(3-oxooctanoyl)-L-homoserine lactone (3OC8HSL), and N-(3-oxododecanoyl)-L-homoserine lactone (3OC12HSL). Furthermore, the application of strain XN-36 as a biocontrol agent could substantially alleviate the soft rot disease caused by P. carotovorum to suppress tissue maceration in a variety of host plants, including Chinese cabbage (Brassica pekinensis(Lour.) Rupr.), carrot (Daucus carota L.) and potato (Solanum tuberosum L.). Similarly, the application of crude enzymes of strain XN-36 significantly attenuated the disease incidence and severity in host plants. Enzyme activity test indicated that strain XN-36 has acylase activity. These findings expand the application of QQ strains as biocontrol agents, while opening up new prospects for the control of QS-mediated bacterial diseases.