Bacterial community-emitted volatiles regulate Arabidopsis growth and root architecture in a distinct manner of those from individual strains

Volatile organic compounds (VOCs) function as infochemicals and are important means of communication between bacteria and plants. Bacterial VOCs can promote plant growth and protect plants against both biotic and abiotic stresses. Most studies to date have focused on VOCs from single bacterial strains; consequently, very little is known about VOCs emitted by bacterial communities and their role in modulating plant phenotypes. In this work, we showed that VOCs from a root-derived 16-strain synthetic community affect Arabidopsis growth and root system architecture, whereas VOCs from individual strains produce a range of different effects. Removal of key species from the community changed the relative abundances of other strains and altered the VOC composition; however, the effect on plant growth remained the same. We therefore concluded that bacterial VOC-induced modulation of plant responses in the rhizosphere may be an emergent property of bacterial communities, rather than merely the sum of effects exerted by individual species. In total, we detected 135 different volatiles from individual strains, with dimethyl disulfide (DMDS) being the most abundant compound emitted by the community. Correlation analysis predicted several sulfur-containing compounds to promote plant growth, and revealed that exposure to two such VOCs, along with DMDS, leads to plant growth promotion. We also identified plant mutants unresponsive to DMDS, suggesting that its mechanism of action may involve assimilation into S-methylcysteine. Finally, we propose that the ecological role of VOCs is to provide early signaling alerts that prime plants for interaction with the bacterial community through modulation of root exudate composition and accumulation of defense compounds, thereby affecting the bacterial colonization of the plants.