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Rhizobia are soil bacteria that can form a symbiosis with legumes. These bacteria induce the formation of new root organs, the nodules, which they colonize massively for a certain time before being released into the soil. In compatible interactions, intracellular bacteria bind atmospheric nitrogen to the plant, converting symbiosis into mutualism.

During evolution, symbiotic modules bearing genes essential for nodulation (nodule formation) and nitrogen fixation propagated to various soil bacteria, giving them a certain degree of symbiotic ability in function of the recipient's genome. The symbiotic characters acquired by gene transfer were then improved under the pressure of plant breeding.

Since colonization of root nodules and nitrogen fixation are not genetically linked, rhizobia can colonize plants without any benefit to them. The emergence of mutualism, resulting from the transfer of symbiotic modules into originally non-symbiotic bacterial populations, and its maintenance during evolution suggest that non-beneficial strains (which do not fix nitrogen) are counter-selected (" sanctioned ").

Where and when are the bacteria unable to fix nitrogen sanctioned?

In this study, LIPM's "symbiotic functions, genome and evolution of rhizobia" team focused on determining where and when bacteria were found to be ineffective in fixing nitrogen during the infectious process. In particular, can plants discriminate fixers and non-fixers within a single nodule? If nitrogen-fixing variants emerge in a population, will this character spread under the selection pressure of the plant and under what conditions?

To answer this question, the researchers followed the number and the viability of two sub-populations (Fix + and Fix-) of the same bacterial population (Cupriavidus taiwanensis) differing only in the presence of a system of functional fixation of nitrogen, during their symbiotic interaction with Mimosa pudica. They find that Fix + and Fix- enter and multiply similarly during the first days, but that Fix + progressively outperforms Fix- during the infectious process. From 19 to 20 days after inoculation, Fix-bacteria and the nodule cells that harbor them specifically degenerate, indicating that control of nitrogen fixation occurs at the post-infection stage and at the nodule cell level.

Mathematical modeling of the dynamics of mutualist and non-mutual populations, and their experimental validation, then made it possible to show that rare Fix + variants invade a population at the start of Fix-, during repeated infectious cycles and under favorable conditions. These conditions are a function of the initial inoculum, the size of the plant population and the length of the nodulation cycle.

This work provides a better understanding of the evolution of mutualism in populations of legume symbionts, that is to say its maintenance and propagation.