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

Abstract

Cyclic lipopeptides are key bioactive secondary metabolites produced by some plant beneficial rhizobacteria such as Pseudomonas and Bacillus. 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 of Bacillus and Pseudomonas cyclic lipopeptides by Streptomyces venezuelae. We observed that Streptomyces is able to degrade the three lipopeptides surfactin, iturin and fengycin upon confrontation with of B. velezensis in vitro and in planta according to specific mechanisms. S. venezuelae was also able to degrade the structurally diverse sessilin, tolaasin, orfamide, xantholisin and putisolvin-type lipopeptides produced by Pseudomonas, 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 enhance Streptomyces growth, indicating a possible nutritional utilization. Thereby, this work stresses on how the enzymatic arsenal of S. venezuelae may contribute to its adaptation to BSMs-driven interactions with microbial competitors. The ability of Streptomyces to degrade exogenous lipopeptides and feed on them adds a new facet to the implications of the degradation of those compounds by Streptomyces, 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 of B. velezensis, avoiding the confrontation zone with Streptomyces and 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.

Does regulation hold the key to optimizing lipopeptide production in Pseudomonas for biotechnology?

“…However, a key outcome of such research to date is the finding that microbial degradation of LPs can result in structural changes that alter their biological activities. For example, in Bacillus , degradation of surfactin generates a linear surfactin which can no longer induce systemic resistance (ISR) in tobacco ( Rigolet et al, 2023 ). Linear surfactant also displays a reduced ability to lower surface tension when compared to cyclic surfactin ( Liu et al, 2015 ).…”

“…More recently ( Hansen et al, 2023 ), reported the cooperative degradation of orfamide A by Rhodococcus globerulus D757 and Stenotrophomonas indicatrix D763 to protect orfamide-sensitive members of a synthetic community during co-culture with the orfamide-producer P. protegens . It has been proposed that degradation of CLPs could be a strategy deployed by competitors to prevent CLP producers from performing “critical” functions in their environment such as biofilm formation, enhancing motility or colonization of specific niches ( Rigolet et al, 2023 ). In another recent study ( Zhang et al, 2021 ), present a new role of LPs in mediating bacterial cooperation to evade amoebal predation.…”

“…Frontiers in Bioengineering and Biotechnology frontiersin.org systemic resistance (ISR) in tobacco (Rigolet et al, 2023). Linear surfactant also displays a reduced ability to lower surface tension when compared to cyclic surfactin (Liu et al, 2015).…”