Transitive interactions among rhizobia determine their symbiotic fitness

Abstract

During host-microbe symbioses, the fitness of mutualistic microbes is determined by the interactions that concurrently occur, throughout their life cycle, with their host and other members of the surrounding microbial community. Disentangling how these multiple interactions shape the fitness of microbial symbionts is challenging, but is essential to understand the diversity and functioning of mutualisms. Here we examined the different fitness components of rhizobial symbionts of the legume plant Mimosa pudica across the multiple stages of their symbiotic life cycle. By comparing rhizobial symbiotic fitness in single and pairwise inoculations, we found that inter-bacterial interactions causing significant fitness effects are common, transitive and can have major consequences, sometimes leading to the extinction of a strain. These interactions predominantly occur at the root infection (nodulation) step, but smaller post-infection interaction effects, involving yet uncharacterized mechanisms, were also detected. Furthermore, considering pairwise interactions was sufficient to predict fitness ranks in more complex rhizobial communities consisting of 6 or 8 strains, indicating that higher-order interaction effects do not play a significant role in these communities. Overall, our results provide a quantitative framework to describe the main drivers of rhizobial symbiotic fitness in a simple community context.