Multigenerational inheritance drives symbiotic interactions of the bacterium Bacillus subtilis with its plant host

Bacillus subtilis is a beneficial bacterium that supports plant growth and protects plants from bacterial, fungal, and viral infections. Using a simplified system of B. subtilis and Arabidopsis thaliana interactions, we studied the fitness and transcriptome of bacteria detached from the root over generations of growth in LB medium. We found that bacteria previously associated with the root or exposed to its secretions had greater stress tolerance and were more competitive in root colonization than bacteria not previously exposed to the root. Furthermore, our transcriptome results provide evidence that plant secretions induce a microbial stress response and fundamentally alter signaling by the cyclic nucleotide c-di-AMP, a signature maintained by their descendants. The changes in cellular physiology due to exposure to plant exudates were multigenerational, as they allowed not only the bacterial cells that colonized a new plant but also their descendants to have an advance over naive competitors of the same species, while the overall plasticity of gene expression and rapid adaptation were maintained. These changes were hereditary but not permanent. Our work demonstrates a bacterial memory manifested by multigenerational reversible adaptation to plant hosts in the form of activation of the stressosome, which confers an advantage to symbiotic bacteria during competition. •Bacillus subtilis is a beneficial bacterium that promotes plant growth and defends plants against pathogens.•Bacillus subtilis cells that have been in contact with the plant's root or its secretions showed better stress tolerance and were more effective at colonizing the roots compared to bacteria that had not been exposed to the root.•Plant exudations but not simple carbons or nitrogen fundamentally alter the transcriptome of the bacteria and their intracellular signaling, a signature maintained by their descendants.•Bacteria develop a "memory" that allows them to adapt to plant hosts over multiple generations through activating the stress response system, giving them an advantage in competition.