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Ongena, M.

Publications and source records attributed to Ongena, M..

8 recordsLinked to original sources

Bacillus adaptation to Pseudomonas secondary metabolites enhances its root competitiveness

Bacillus velezensis is a widely used plant growth-promoting rhizobacterium whose effectiveness under natural conditions is strongly influenced by interactions with surrounding microorganisms. While bacterial secondary metabolites are known to shape these interactions, little is known about their long-term evolutionary consequences. Here, we show that repeated exposure of B. velezensis GA1 to secondary metabolites produced by the competing rhizobacterium Pseudomonas sessilinigenes CMR12a drives the emergence of an adapted subpopulation with enhanced ecological fitness. Multi-omics analyses revealed extensive metabolomic and transcriptional changes associated with altered growth dynamics, sporulation, motility, and biofilm formation. Importantly, the evolved variant exhibited improved tomato root colonization and reduced the abundance of the competing Pseudomonas strain in planta. Together, our results demonstrate that prolonged exposure to diffusible bacterial metabolites can drive rapid adaptive diversification in rhizosphere-associated bacteria and highlight the importance of long-term interbacterial interactions in shaping the outcome of plant microbiome assembly and biocontrol performance.

microbiology↗

A bacterial lipid triggers membrane mechanosensing immunity in Arabidopsis

The plant immune system engages cell-surface receptors that detect microbe-associated molecular patterns to initiate pattern-triggered immunity (PTI), and intracellular receptors that sense microbe-secreted effectors to activate effector-triggered immunity (ETI). Whether additional modes of microbial detection exist remains unclear. Here, we define membrane mechanosensing immunity (MSI), a third layer of immune signaling. A bacterial lipid, the main diffusible signal factor (DSF) from Xanthomonas campestris pv. campestris, acts as a membrane-active molecule that alters plasma membrane biophysical properties, activates Mechanosensitive Channel of Small Conductance (MscS)-like (MSL)-dependent immune signaling, and triggers a broad transcriptional reprogramming that overlaps with PTI and ETI. MSI modulates PTI signaling and requires both PTI and ETI components for effective disease resistance. These findings establish the sensing of metabolite-induced membrane perturbations as a mechanism of microbial detection.

plant biology↗

Nitrogen sources enhance siderophore-mediated competition for iron between potato common scab and late blight causative agents

Withdrawal StatementThe authors have withdrawn their manuscript owing to the fact that the P. infestans strain received from third parties is not the one referred in the manuscript despite having the certificate from the providing collection. All the experiments and data are correct but not included into a proper research context. A new version of this work will be published in near future. Therefore, the authors do not wish this work to be cited as reference for the project. If you have any questions, please contact the corresponding author.

microbiology↗

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

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.

microbiology↗

Mechanosensing and Sphingolipid-Docking Mediate Lipopetide-Induced Immunity in Arabidopsis

Bacteria-derived lipopeptides are immunogenic triggers of host defenses in metazoans and plants. Root-associated rhizobacteria produce cyclic lipopeptides that activate systemically induced resistance (IR) against microbial infection in various plants. How these molecules are perceived by plant cells remains elusive. Here, we reveal that immunity activation in Arabidopsis thaliana by the lipopeptide elicitor surfactin is mediated by docking into specific sphingolipid-enriched domains and relies on host membrane deformation and subsequent activation of mechanosensitive ion channels. This mechanism leads to host defense potentiation and resistance to the necrotroph B. cinerea but is distinct from host pattern recognition receptor-mediated immune activation and reminiscent of damage-induced plant immunity.

plant biology↗

Chelator sensing and lipopeptide interplay mediates molecular interspecies interactions between soil bacilli and pseudomonads

AbstractSome bacterial species are important members of the rhizosphere microbiome and confer protection to the host plant against pathogens. However, our knowledge of the multitrophic interactions determining the ecological fitness of these biocontrol bacteria in their highly competitive natural niche is still limited. In this work, we 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 enantio-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 but, unexpectedly, the lipopeptide also acts as a chemical trap that reduces the toxicity of other lipopeptides released by Pseudomonas challengers. This in turn 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.

microbiology↗

Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of Bacillus-plant mutualistic interaction

Bacillus velezensis is considered as model species belonging to the so-called B. subtilis complex that typically evolved to dwell in the soil rhizosphere niche and establish intimate association with plant roots. This bacterium provides protection to its natural host against diseases and represents one of the most promising biocontrol agents. However, the molecular basis of the cross-talk that this bacterium establishes with its natural host has been poorly investigated. We show here that these plant-associated bacteria have evolved some polymer-sensing system to perceive their host and that in response, they increase the production of the surfactin-type lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favoured upon growth on root exudates and that this lipopeptide is a key component used by the bacterium to optimize biofilm formation, motility and early root colonization. In this specific nutritional context, the bacterium also modulates qualitatively the pattern of surfactin homologues co-produced in planta and mainly forms variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. ImportanceWithin the plant-associated microbiome, some bacterial species are of particular interest due to the disease protective effect they provide via direct pathogen suppression and/or stimulation of host immunity. While these biocontrol mechanisms are quite well characterized, we still poorly understand the molecular basis of the cross talk these beneficial bacteria initiate with their host. Here we show that the model species Bacillus velezensis stimulates production of the surfactin lipopeptide upon sensing pectin as cell surface molecular pattern and upon feeding on root exudates. Surfactin favors bacterial rhizosphere fitness on one hand and primes the plant immune system on the other hand. Our data therefore illustrate how both partners use this multifunctional compound as unique shared good to sustain mutualistic interaction.

microbiology↗

Rhamnolipids and their 3-(3-hydroxyalkanoyloxy)alkanoic acid precursors activate Arabidopsis innate immunity through two independent mechanisms

Plant innate immunity is activated upon perception of invasion pattern molecules by plant cell-surface immune receptors. Several bacteria of the genera Pseudomonas and Burkholderia produce rhamnolipids (RLs) from L- rhamnose and (R)-3-hydroxyalkanoate precursors (HAAs). RL and HAA secretion is required to modulate bacterial surface motility, biofilm development, and thus successful colonization of hosts. Here, we show that the lipidic secretome from the opportunistic pathogen Pseudomonas aeruginosa mostly comprising RLs and HAAs stimulates Arabidopsis immunity. We demonstrate that HAAs are sensed by the bulb-type lectin receptor kinase LIPOOLIGOSACCHARIDE-SPECIFIC REDUCED ELICITATION/S-DOMAIN-1-29 (LORE/SD1-29) that also mediates medium-chain 3-hydroxy fatty acid (mc-3-OH-FA) perception in the plant Arabidopsis thaliana. HAA sensing induces canonical immune signaling and local resistance to plant pathogenic Pseudomonas infection. By contrast, RLs trigger an atypical immune response and resistance to Pseudomonas infection independent of LORE. Thus, the glycosyl moieties of RLs, albeit abolishing sensing by LORE, do not impair their ability to trigger plant defense. In addition, our results show that RL-triggered immune response is affected by the sphingolipid composition of the plasma membrane. In conclusion, RLs and their precursors released by bacteria can both be perceived by plants but through distinct mechanisms. SignificanceActivation of plant innate immunity relies on the perception of microorganisms through self and nonself elicitors. Rhamnolipids and their precursor HAAs are exoproducts produced by beneficial and pathogenic bacteria. They are involved in bacterial surface dissemination and biofilm development. As these compounds are released in the extracellular milieu, they have the potential to be perceived by the plant immune system. Our work shows that both compounds independently activate plant immunity. We demonstrate that HAAs are perceived by the receptor protein kinase LORE. By contrast, rhamnolipids are not senses by LORE but activate a non-canonical immune response affected by the sphingolipid composition of the plant plasma membrane. Thus, plants are able to sense bacterial molecules as well as their direct precursors to trigger a distinct immune response.

plant biology↗