Bacillus spp. strains that are beneficial to plants are widely used in commercial biofertilizers and biocontrol agents for sustainable agriculture. Generally, functional Bacillus strains are applied as single strain communities since the principles of synthetic microbial consortia constructed with Bacillus strains remain largely unclear. Here, we demonstrated that the kin discrimination system directly affects the survival and function of two-member consortia composed of B. velezensis SQR9 and FZB42 in the rhizosphere. A mutation in the global regulator Spo0A of SQR9 markedly reduced the boundary phenotype with wild-type FZB42, and the combined use of the spo0A mutant and FZB42 improved biofilm formation, root colonization and the production of secondary metabolites that are beneficial to plants. We further confirmed the correlation between the swarm discrimination phenotype within community members and effects that are beneficial to plants in greenhouse experiments. Our results provide evidence that social interactions among bacteria could be an influencing factor in achieving a desired community-level function.

Lateral root (LR) formation is coordinated by both endogenous and external factors. As biotic factors, Plant growth-promoting rhizobacteria (PGPRs) can affect LR formation, while the regulation mechanism is unclear. In this study, by applying various marker lines, we found that volatile compounds (VCs) from PGPR strain Bacillus amyloliquefaciens SQR9 induced a high frequency of oscillation and prebranch site formation, and further accelerated the development and emergence of the lateral root primordia (LRP), thus promoting LR development in model plant Arabidopsis. We demonstrated a critical role of auxin on SQR9 VCs-induced lateral root formation via respective mutants and pharmacological experiments. Our results showed that the YUC9 (YUCs)-mediated auxin biosynthesis, polar auxin transport, and auxin signaling pathway are involved in SQR9 VCs-induced LRs formation. We further showed that acetoin, a major component of SQR9 VCs, is less active in promoting root development compared to SQR9 cells, suggesting uncharacterized VCs might contribute to SQR9 effect in mediating LR formation. In summary, our study revealed a novel mechanism of PGPR-produced VCs in regulating LR branching in a non-contact manner, and further efforts will explore useful VCs to promote plant root development.