Bacillus subtilis (B. subtilis) is a plant growth promoter and a biocontrol agent that supports plant growth and protects it from bacterial, fungal, and viral infections. These bacteria and related species are well adapted to extreme environments and offer an unexploited reservoir for bio-fertilizers and bio-control agents against various abiotic and biotic stresses that endanger diverse agricultural ecosystems. Here, we propose that history-dependent behavior is an essential manifestation of plant colonization in extreme abiotic stresses, such as drought and salinity, worth classifying and quantifying. To study history-dependent adaptation to plant hosts, we developed a simple framework for measuring the physiological memory of B. subtilis about past interactions with the plant.
We found that A. thaliana secretions reduce the lag time in pre-exposed bacteria compared with naïve B. subtilis cells, even after their complete removal. Pre-exposed B. subtilis cells colonized plant roots more efficiently than naïve bacteria, were more resistant to salicylic acid, increased salinity, and had an advantage in the competition for root colonization against naïve colonizers. Transcriptome analysis of both ancestors and descendants revealed that a specific core of plant-induced processes, including c-di-AMP signaling, and the general stress response, maintain the signature of association with the plant in descendants of pre-exposed bacteria. Consistently, plant secretions compensated for losing a c-di-AMP diadenylate cyclase but required the general stress response and the master regulator Spo0A to exert their short and long-term effects.
Overall, our work demonstrates that bacterial memory manifested by long-term adaptation to plant hosts confirms an advantage to symbiotic bacteria during competition and survival of extreme abiotic stress.