Plant-mediated selection of endosymbiotic bacteria – SELECT

Eukaryotic organisms are exposed to complex microbial communities that affect their health, development and evolution. They have evolved multiple layers of control mechanisms to defend themselves from pathogens while, at the same time, allowing colonization by beneficial microbes. The filtering of microbes by eukaryotes imposes strong selective constraints on microbial populations and shape their eco-evolutionary dynamics. It is thus important to describe the effect of host-mediated selection on microbial populations to understand, and possibly predict, the evolution of pathogenic and beneficial microorganisms.

The rhizobium-legume symbiosis has a major impact on natural and agricultural ecosystems, contributing to a substantial part of the global flux of nitrogen. During this symbiosis, rhizobia are hosted within specific root organs (called nodules) where they fix atmospheric nitrogen and provide organic ammonium to the plant in exchange for carbon sources. Large phenotypic variations are observed among the different strains that can be found in soil rhizobial populations, some strains being highly beneficial while others provide little or no nitrogen to their host. During the interaction with the plant, rhizobial fitness is determined by the realization of three symbiotic steps: nodulation, leading to formation of new plant organs; infection, the entry and proliferation of bacteria within plant cells; and nitrogen fixation and the provision of ammonium to the plant. These three steps are jointly controlled by the genotypes of the two partners and influenced by ecological conditions, including the complexity of the rhizobial community in the rhizosphere.

SELECT will study how plant-mediated selection shapes bacterial fitness and the evolution of phenotypic traits involved in the different symbiotic steps. Three complementary experimental systems will be exploited to investigate different facets of this question. First, an evolution experiment that recapitulates in the laboratory the emergence of new rhizobia from a pathogenic ancestor will be analyzed to describe the dynamics of phenotypic and genetic evolution leading to the acquisition and improvement of the first two symbiotic steps, nodulation and infection. Next, I will genetically engineer rhizobia that fix different amounts of nitrogen to establish the quantitative relationship between nitrogen fixation and bacterial fitness within nodules. Last, I will use a collection natural rhizobial strains to compare the expression and evolution of symbiotic phenotypes after the inoculation of one or multiple bacterial strains on the host plant. The different experimental results will be integrated through mathematical modelling to analyze the relative contribution of the different symbiotic steps on bacterial fitness.

Overall, SELECT will thus couple several approaches (from bacterial genetics and genomics to experimental evolution and mathematical modelling) and experimental systems to provide a detailed view of the factors determining bacterial fitness during a complex mutualistic interaction. The fundamental insights on the eco-evolutionary dynamics of host-associated bacteria generated during SELECT may contribute, on the longer term, to improve agro-ecological practices by allowing the development of selection procedures to improve rhizobial performances (both nodulation competitiveness and nitrogen fixation efficiency) under different ecological contexts and on different host plants.