Wheat Metabolite Interferences on Fluorescent Pseudomonas Physiology Modify Wheat Metabolome through an Ecological Feedback.

Plant roots exude a wide variety of secondary metabolites able to attract and/or control a large diversity of microbial species. In return, among the root microbiota, some bacteria can promote plant development. Among these, Pseudomonas are known to produce a wide diversity of secondary metabolites that could have biological activity on the host plant and other soil microorganisms. We previously showed that wheat can interfere with Pseudomonas secondary metabolism production through its root metabolites. Interestingly, production of Pseudomonas bioactive metabolites, such as phloroglucinol, phenazines, pyrrolnitrin, or acyl homoserine lactones, are modified in the presence of wheat root extracts. A new cross metabolomic approach was then performed to evaluate if wheat metabolic interferences on Pseudomonas secondary metabolites production have consequences on wheat metabolome itself. Two different Pseudomonas strains were conditioned by wheat root extracts from two genotypes, leading to modification of bacterial secondary metabolites production. Bacterial cells were then inoculated on each wheat genotypes. Then, wheat root metabolomes were analyzed by untargeted metabolomic, and metabolites from the Adular genotype were characterized by molecular network. This allows us to evaluate if wheat differently recognizes the bacterial cells that have already been into contact with plants and highlights bioactive metabolites involved in wheat-Pseudomonas interaction.

A Cross-Metabolomic Approach Shows that Wheat Interferes with Fluorescent Pseudomonas Physiology through Its Root Metabolites.

Roots contain a wide variety of secondary metabolites. Some of them are exudated in the rhizosphere, where they are able to attract and/or control a large diversity of microbial species. In return, the rhizomicrobiota can promote plant health and development. Some rhizobacteria belonging to the Pseudomonas genus are known to produce a wide diversity of secondary metabolites that can exert a biological activity on the host plant and on other soil microorganisms. Nevertheless, the impact of the host plant on the production of bioactive metabolites by Pseudomonas is still poorly understood. To characterize the impact of plants on the secondary metabolism of Pseudomonas, a cross-metabolomic approach has been developed. Five different fluorescent Pseudomonas strains were thus cultivated in the presence of a low concentration of wheat root extracts recovered from three wheat genotypes. Analysis of our metabolomic workflow revealed that the production of several Pseudomonas secondary metabolites was significantly modulated when bacteria were cultivated with root extracts, including metabolites involved in plant-beneficial properties.

Secondary metabolites from plant-associated Pseudomonas are overproduced in biofilm.

Plant rhizosphere soil houses complex microbial communities in which microorganisms are often involved in intraspecies as well as interspecies and inter-kingdom signalling networks. Some members of these networks can improve plant health thanks to an important diversity of bioactive secondary metabolites. In this competitive environment, the ability to form biofilms may provide major advantages to microorganisms. With the aim of highlighting the impact of bacterial lifestyle on secondary metabolites production, we performed a metabolomic analysis on four fluorescent Pseudomonas strains cultivated in planktonic and biofilm colony conditions. The untargeted metabolomic analysis led to the detection of hundreds of secondary metabolites in culture extracts. Comparison between biofilm and planktonic conditions showed that bacterial lifestyle is a key factor influencing Pseudomonas metabolome. More than 50% of the detected metabolites were differentially produced according to planktonic or biofilm lifestyles, with the four Pseudomonas strains overproducing several secondary metabolites in biofilm conditions. In parallel, metabolomic analysis associated with genomic prediction and a molecular networking approach enabled us to evaluate the impact of bacterial lifestyle on chemically identified secondary metabolites, more precisely involved in microbial interactions and plant-growth promotion. Notably, this work highlights the major effect of biofilm lifestyle on acyl-homoserine lactone and phenazine production in P. chlororaphis strains.

Exploiting rhizosphere microbial cooperation for developing sustainable agriculture strategies.

The rhizosphere hosts a considerable microbial community. Among that community, bacteria called plant growth-promoting rhizobacteria (PGPR) can promote plant growth and defense against diseases using diverse distinct plant-beneficial functions. Crop inoculation with PGPR could allow to reduce the use of pesticides and fertilizers in agrosystems. However, microbial crop protection and growth stimulation would be more efficient if cooperation between rhizosphere bacterial populations was taken into account when developing biocontrol agents and biostimulants. Rhizospheric bacteria live in multi-species biofilms formed all along the root surface or sometimes inside the plants (i.e., endophyte). PGPR cooperate with their host plants and also with other microbial populations inside biofilms. These interactions are mediated by a large diversity of microbial metabolites and physical signals that trigger cell-cell communication and appropriate responses. A better understanding of bacterial behavior and microbial cooperation in the rhizosphere could allow for a more successful use of bacteria in sustainable agriculture. This review presents an ecological view of microbial cooperation in agrosystems and lays the emphasis on the main microbial metabolites involved in microbial cooperation, plant health protection, and plant growth stimulation. Eco-friendly inoculant consortia that will foster microbe-microbe and microbe-plant cooperation can be developed to promote crop growth and restore biodiversity and functions lost in agrosystems.