The fate of bacterial secondary metabolites in the rhizosphere:Streptomycesdegrades and feeds on cyclic lipopeptides produced by competitors

Abstract

AbstractCyclic lipopeptides are key bioactive secondary metabolites produced by some plant beneficial rhizobacteria such asPseudomonasandBacillus. They exhibit antimicrobial properties, promote induced systemic resistance in plants and support key developmental traits including motility, biofilm formation and root colonization. However, our knowledge about the fate of lipopeptides once released in the environment and especially upon contact with neighboring rhizobacteria remains limited. Here, we investigated the enzymatic degradation ofBacillusandPseudomonascyclic lipopeptides byStreptomyces venezuelae. We observed thatStreptomycesis able to degrade the three lipopeptides surfactin, iturin and fengycin upon confrontation with ofB. velezensis in vitroandin plantaaccording to specific mechanisms.S. venezuelaewas also able to degrade the structurally diverse sessilin, tolaasin, orfamide, xantholisin and putisolvin-type lipopeptides produced byPseudomonas, indicating that this trait is likely engage in the interaction with various competitors.Furthermore, the degradation of CLPs is associated with the release of free amino and fatty acids and was found to enhanceStreptomycesgrowth, indicating a possible nutritional utilization. Thereby, this work stresses on how the enzymatic arsenal ofS. venezuelaemay contribute to its adaptation to BSMs-driven interactions with microbial competitors. The ability ofStreptomycesto degrade exogenous lipopeptides and feed on them adds a new facet to the implications of the degradation of those compounds byStreptomyces, where linearization of surfactin was previously reported as a detoxification mechanism. Additionally, we hypothesize that lipopeptide-producing rhizobacteria and their biocontrol potential are impacted by the degradation of their lipopeptides as observed with the polarized motility ofB. velezensis, avoiding the confrontation zone withStreptomycesand the loss of antifungal properties of degraded iturin. This work illustrates how CLPs, once released in the environment, may rapidly be remodeled or degraded by members of the bacterial community, with potential impacts on CLP-producing rhizobacteria and the biocontrol products derived from them.