Bacterial Volatile Organic Compounds Mediate a Cooperative Relationship Between Bacteria and Plants Under Heavy Metal Stress

Abstract

Bacterial volatile organic compounds (BVOCs) are increasingly recognised as effective signalling molecules that stimulate plant growth and stress responses. Although BVOC production may impose metabolic costs on bacteria, the benefits gained by VOC‐emitting bacteria through BVOC‐mediated communication with plants remain unclear. In this study, we established Pb‐stressed conditions for Bacillus megaterium, Arabidopsis thaliana or both organisms to investigate their reciprocal interactions. Pb‐stressed bacteria emitted a distinct VOC profile and exhibited significant reprogramming of sugar and nitrogen‐containing carbon metabolism compared with unstressed bacteria. Plant growth inhibition caused by Pb was alleviated by VOCs emitted from unstressed bacteria; however, this alleviation was enhanced by 36% when the bacteria were exposed to Pb stress, indicating that Pb‐induced changes in bacterial VOC metabolism trigger distinct plant responses. Specifically, Pb accumulation increased by up to 95% in plant shoot, whereas oxidative damage markers, including malondialdehyde and H2O2, decreased by up to 25% in plants exposed to VOCs from Pb‐stressed bacteria compared with those exposed to VOCs from Pb‐unstressed bacteria. These effects were associated with increased expression of antioxidant enzyme‐related genes in plants exposed to VOCs from Pb‐stressed bacteria. Finally, we confirmed that the Pb‐stressed bacteria‐mediated increases in plant growth and Pb uptake were accompanied by alleviation of the Pb stress‐induced reduction in bacterial population. Overall, our results demonstrate that VOC‐emitting bacteria can benefit from modulating plant physiology and suggest that a cooperative relationship between bacteria and plants can be established through BVOC‐mediated communication.