Nutrient Availability Modulates Beneficial Effect of Bacterial Community Volatiles and Contact-Dependent Interactions Differently

Plant growth-promoting bacteria enhance plant performance, yet how different modes of plant-microbe interaction shape nutrient-specific host responses remains poorly understood. In particular, it is unclear how direct bacterial contact and volatile-mediated interactions originating from the same bacterial community differentially regulate plant nutrient acquisition pathways. Here, we investigated how a 16-member synthetic bacterial community (16SC) affects plant growth, nutrient status, signaling, and metabolite profiles under full nutrient supply as well as nitrogen (N), sulfur (S), and phosphorus (P) limitation in Arabidopsis thaliana. We show that volatile organic compounds (VOCs) emitted by the 16SC promote shoot growth under nitrate limitation and full nutrient conditions, whereas this growth promotion is lost under sulfur- and phosphorus-limiting conditions. In contrast, direct interaction (DBC) between plants and the 16SC abolishes growth promotion under all three nutrient-limiting conditions. These nutrient-dependent phenotypes correlate with distinct regulation of nutrient transporters and key transcriptional regulators involved in N (NRT1;1 / NLP7), S (SULTR1;2 / SLIM1/EIL3), and P (PHO2 / PHR1) signaling pathways. Genetic analyses using nutrient transporter mutants revealed that VOC-induced growth promotion requires functional NRT1;1 and SULTR1;2 transporters, whereas growth promotion mediated by direct bacterial contact is retained in the corresponding mutants. This uncoupling of VOC- and contact-dependent effects indicates that distinct host regulatory pathways underlie bacterial community growth promotion depending on the interaction mode. Together, our findings demonstrate that bacterial community-mediated plant growth promotion is strongly shaped by nutrient context and interaction mode, and that volatile-mediated and contact-dependent mechanisms engage separable host nutrient regulatory networks.