Bacterial Strain Identity and Community Composition Drive the Seed-to-Seedling Microbiota Assembly

Abstract The seed-to-seedling transition is a key step of plant microbiota assembly, where the seed microbiota meets the soil microbiota. Seed germination triggers profound physiological changes, including exudate release and oxidative bursts, which generate selective pressures shaping microbial survival and interactions. Here, we investigated how host selection and community composition influence bacterial colonization during this transition using a Synthetic Community (SynCom) approach on common bean ( Phaseolus vulgaris ) seeds. Specifically, we tested the importance of microbial interactions by applying 30 bacterial SynComs spawning a phylogenetic diversity gradient. Seedling colonization success was primarily determined by strain identity but was strongly modulated by the SynCom context. Strains that were highly effective colonizers when inoculated alone often exhibited reduced transmission within SynComs, indicating that microbial interactions can either inhibit or facilitate colonization. Random forest models confirmed that colonization outcomes could not be predicted from single-strain performance alone. Instead, both phylogenetic relatedness and metabolic similarity among SynCom members emerged as key predictors of strain success, supporting the competition–relatedness hypothesis and highlighting the importance of community-dependent effects in shaping colonization success. Genomic analyses identified microbial traits linked to efficient seedling colonization, notably amino acid transport and metabolism, stress tolerance, ROS detoxification, and biofilm formation, highlighting the strong selective pressures acting during the seed-to-seedling transition. Besides key adaptative traits, our findings underscore the importance of microbial interactions to survive and colonize seedlings, bringing a novel perspective for the successful engineering of seed and seedling microbiota.