Abstract

Interactions between plant pathogens and root-associated microbes play an important role in determining disease outcomes. While several studies have suggested that steering these interactions may improve plant health, such approaches have remained challenging in practice. Because of low iron availability in most soils, competition for iron via secreted siderophore molecules might influence microbial interaction outcomes. Here, we tested if bacterial interactions mediated by iron-scavenging siderophores can be used to predict the disease suppressiveness of microbial consortia against soilborne Ralstonia solanacearum, a bacterial pathogen in the tomato rhizosphere. Iron availability significantly affected the interactions within inoculated consortia and between the consortia and the pathogen. We observed contrasting effects of siderophores and other nonsiderophore metabolites on the pathogen growth, while the siderophore effects were relatively much stronger. Specifically, disease incidence was reduced in vivo when the inoculated consortia produced siderophores that the pathogen could not use for its own growth. Employing siderophore-mediated interactions to engineer functionally robust microbial inoculants shows promise in protecting plants from soilborne pathogens.IMPORTANCE Soil-borne pathogens cause high losses in crop yields globally. The development of environmentally friendly approaches is urgently needed, but is often constrained by complex interactions between root-associated microbes and pathogens. Here, we demonstrate that the interactions within microbial consortia mediated by iron-scavenging siderophores play an important role in reducing pathogen infection and enhancing plant health. This study provides a promising and novel research direction for dealing with a wide range of microbial infections through iron exploitation, which is important for the colonization and infection of both plant and human hosts by pathogens.

Highlights

  • Interactions between plant pathogens and root-associated microbes play an important role in determining disease outcomes

  • The presence of strains R. pickettii QL-A6 and R. taiwanensis QL-117 reduced the lag time, strains R. mannitolilytica QL-A3 and R. pickettii QL-140 increased the lag time, and the strain R. mannitolilytica QL-A2 had a nonsignificant effect (Table S4). These results suggest that siderophore-mediated effects on disease incidence were stronger compared to nonsiderophore metabolite-mediated effects, while these effects varied depending on the stage of infection and the presence of certain species in the inoculated consortium

  • As iron is often an important limiting resource in soil, we hypothesized that bacterial interactions mediated by ironscavenging siderophores could be used to predict the disease suppressiveness and success of microbial inoculants

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Summary

Introduction

Interactions between plant pathogens and root-associated microbes play an important role in determining disease outcomes. We demonstrate that the interactions within microbial consortia mediated by iron-scavenging siderophores play an important role in reducing pathogen infection and enhancing plant health. One environmentally sustainable way to improve plant health is to take advantage of plant-associated microorganisms that form the first line of defense against pathogens by preventing their growth and subsequent virulence [2,3,4,5] The functionality of these natural communities is often compromised in agricultural soils due to the extinction of several beneficial strains via high-intensity agricultural practices [6, 7]. Metabolic interactions and resource competition have been shown to be important in determining pathogen infections in the soil [18, 19], and how these interactions take place within the inoculated consortium and between the consortium and the pathogen is often essential for predicting disease outcomes [12]. We tested if siderophore-mediated interactions between inoculated consortia and the pathogen can be used as an efficient strategy to design suppressive microbial inoculants

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