Tapping the rhizosphere metabolites for the prebiotic control of soil-borne bacterial wilt disease

Abstract

Prebiotics are compounds that selectively stimulate the growth and activity of beneficial microorganisms. The use of prebiotics is a well-established strategy for managing human gut health. This concept can also be extended to plants where plant rhizosphere microbiomes can improve the nutrient acquisition and disease resistance. However, we lack effective strategies for choosing metabolites to elicit the desired impacts on plant health. In this study, we target the rhizosphere of tomato (Solanum lycopersicum) suffering from wilt disease (caused by Ralstonia solanacearum) as source for potential prebiotic metabolites. We identify metabolites (ribose, lactic acid, xylose, mannose, maltose, gluconolactone, and ribitol) exclusively used by soil commensal bacteria (not positively correlated with R. solanacearum) but not efficiently used by the pathogen in vitro. Metabolites application in the soil with 1 µmol g−1 soil effectively protects tomato and other Solanaceae crops, pepper (Capsicum annuum) and eggplant (Solanum melongena), from pathogen invasion. After adding prebiotics, the rhizosphere soil microbiome exhibits enrichment of pathways related to carbon metabolism and autotoxin degradation, which were driven by commensal microbes. Collectively, we propose a novel pathway for mining metabolites from the rhizosphere soil and their use as prebiotics to help control soil-borne bacterial wilt diseases.

Deciphering Microbial Community and Nitrogen Fixation in the Legume Rhizosphere

“…Microbial inoculants have the potential to enhance crop productivity . However, there is a limitation: current microbial inoculant products rely on single microbial species and strains, which can limit their effectiveness owing to environmental variability and competition with native microbes . Researchers have conducted targeted engineering of microbial communities by combining microbiota with diverse functions to overcome this limitation and yield more versatile products .…”

Rhizosphere Mysteries: Metabolite Reduction Down-regulated Fungal Diversity and Community Function

“…In recent years, synthetic microbial communities (SynComs) of varied complexity have been constructed using bottom-up combinations and have been applied to plants as a means to study various aspects of plant microbiome interactions, including elucidation of the specific mechanisms that drive community assembly and the interactions among different members(32). Within this concept, functional keystone species can be predicted through topological networks derived from interactions and through metabolic models(33). This approach provides a pathway to maximize SynCom persistence and trait expression success in natural settings.…”

Innate Root Exudates Contributed to Contrasting Coping Strategies in Response to Ralstonia solanacearum in Resistant and Susceptible Tomato Cultivars

“…Once in contact with a host plant, R. solanacearum can invade the vascular system from the roots or stem base, blocking or damaging the vascular bundle tissue of the host through proliferation and a series of biochemical activities, ultimately leading to plant dehydration and wilt . The rhizosphere provides the basic conditions to support the growth of pathogens, and the rhizosphere metabolites and microorganisms are key factors affecting the migration of R. solanacearum to the root surface and the infection of roots. − As a soil-borne plant disease, the occurrence and prevalence of bacterial wilt are closely related to the physical and chemical properties of the soil . Under continuous cropping conditions, soil acidification, nutrient imbalance, decreased enzyme activity, and soil microbial imbalance promote the growth of R. solanacearum , exacerbating the occurrence of bacterial wilt. , Correspondingly, agricultural and biological measures such as screening resistant cultivars, bio-organic fertilizer application, probiotics, and soil improvement have been developed to alleviate bacterial wilt. − Among these measures, the cultivation of resistant cultivars is the most appropriate and eco-friendly way to control soil-borne diseases .…”

“…Root exudates can alter the physicochemical properties of rhizosphere soil, contributing to the distinct difference between rhizosphere soil and bulk soil . It has been well documented that root exudates regulate R. solanacearum infection through chemotaxis and shaping rhizosphere communities. ,− In terms of specific root exudates, cinnamic, myristic, and fumaric acids mediated chemotaxis and biofilm formation induces the root colonization of R. solanacearum . Compared to sugars and phenolic acids, organic acids and amino acids typically reduce microbial diversity, while amino acids and nitrogen-containing compounds exacerbate bacterial wilt .…”

“…The “cry for help” hypothesis provides a mechanistic explanation for the previously described feedback response of soil to plant diseases, such as the ability of the soil to become disease-resistant soil under the continuous cultivation of diseased plants . Previous studies on the interaction of root exudates with R. solanacearum have mainly focused on exploring the response of root exudates to pathogen invasion. ,,,, For example, a high abundance of R. solanacearum downregulated rhizosphere soil metabolites such as melibiose, sucrose, and fructose . Thus, under the stress of R. solanacearum , the quantity and composition of root exudates undergo changes that may differ significantly from their innate status.…”