Plant-associated Bacillus velezensis and Pseudomonas spp. represent excellent model species as strong producers of bioactive metabolites involved in phytopathogen inhibition and the elicitation of plant immunity. However, the ecological role of these metabolites during microbial interspecies interactions and the way their expression may be modulated under naturally competitive soil conditions has been poorly investigated.
Bacillus velezensis is considered as model species for plant-associated bacilli providing benefits to its host such as protection against phytopathogens. This is mainly due to the potential to secrete a wide range of secondary metabolites with specific and complementary bioactivities. This metabolite arsenal has been quite well defined genetically and chemically but much remains to be explored regarding how it is expressed under natural conditions and notably how it can be modulated upon interspecies interactions in the competitive rhizosphere niche. Here, we show that B. velezensis can mobilize a substantial part of its metabolome upon the perception of Pseudomonas, as a soil-dwelling competitor. This metabolite response reflects a multimodal defensive strategy as it includes polyketides and the bacteriocin amylocyclicin, with broad antibiotic activity, as well as surfactin lipopeptides, contributing to biofilm formation and enhanced motility. Furthermore, we identified the secondary Pseudomonas siderophore pyochelin as an info-chemical, which triggers this response via a mechanism independent of iron stress. We hypothesize that B. velezensis relies on such chelator sensing to accurately identify competitors, illustrating a new facet of siderophore-mediated interactions beyond the concept of competition for iron and siderophore piracy. This phenomenon may thus represent a new component of the microbial conversations driving the behavior of members of the rhizosphere community.
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.
Some bacterial species are important members of the rhizosphere microbiome and confer protection to the host plant against pathogens. However, our knowledge is still limited about the multitrophic interactions determining the ecological fitness of these biocontrol bacteria in their highly competitive natural niche. In this work, we have investigated the molecular mechanisms underlying interactions between B. velezensis, considered as model plant-associated and beneficial species in the Bacillus genus, and Pseudomonas as a rhizosphere-dwelling competitor. Our data show that B. velezensis boosts its arsenal of specialized antibacterials upon the perception of the secondary siderophore pyochelin produced by phylogenetically distinct pseudomonads and some other genera. We postulate that B. velezensis has developed some chelator sensing systems to learn about the identity of its surrounding competitors. Illustrating the multifaceted molecular response of Bacillus, surfactin is another crucial component of the secondary metabolome mobilized in interbacteria competition. Its accumulation not only enhances motility capability but, unexpectedly, this lipopeptide also acts as a chemical trap that reduce the toxicity of other lipopeptides released by Pseudomonas challengers. This favors the persistence of Bacillus populations upon competitive root colonization. Our work thus highlights new ecological roles for bacterial secondary metabolites acting as key drivers of social interactions.
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