Diverse effects of Bacillus sp. NYG5-emitted volatile organic compounds on plant growth, rhizosphere microbiome, and soil chemistry

Abstract

Bacterial strains in the rhizosphere secrete volatile organic compounds (VOCs) that play critical roles in inter- and intra-kingdom signaling, influencing both microbe-microbe and microbe-plant interactions. In this study we evaluated the plant growth-promoting effects of VOCs emitted by Bacillus sp. NYG5 on Arabidopsis thaliana, Nicotiana tabacum, and Cucumis sativus, focusing on VOC-induced alterations in plant metabolic pathways, rhizosphere microbial communities, and soil chemical properties. NYG5 VOCs enhanced plant biomass across all tested species and induced significant shifts in rhizosphere microbial community composition, specifically increasing relative abundance of Gammaproteobacteria and reducing Deltaproteobacteria (Linear discriminant analysis Effect Size, p < 0.05). Soil analysis revealed a considerable reduction in humic substance concentrations following VOCs exposure, as detected by fluorescent spectral analysis. Using SPME-GC-MS, several novel VOCs were identified, some of which directly promoted plant growth. Transcriptomic analysis of N. tabacum exposed to NYG5 VOCs demonstrated activation of pathways related to phenylpropanoid biosynthesis, sugar metabolism, and hormone signal transduction. Within the phenylpropanoid biosynthesis pathway, a significant upregulation (p adj = 1.16e-14) of caffeic acid 3-O-methyltransferase was observed, a key enzyme leading to lignin and suberin monomer biosynthesis. These results highlight the complex mechanisms through which bacterial VOCs influence plant growth, including metabolic modulation, rhizosphere microbiome restructuring, and soil chemical changes. Collectively, this study highlights the pivotal role of bacterial VOCs in shaping plant-microbe-soil interactions.