Root-derived low molecular weight organic acids modulate keystone microbial taxa impacting plant phosphorus acquisition

Low-molecular-weight organic acids (LMWOAs) present in root exudates modulate the assembly and function of phosphorus (P)-mobilizing bacteria in the rhizosphere. Nonetheless, relatively little is known about how specific LMWOAs affect the structure of rhizosphere microbes associated with P cycling. This study aimed to elucidate the mechanisms by which LMWOAs affect the recruitment of P-mobilizing bacterial communities, with implications for P bioavailability and plant P uptake. The pqqC and phoD bacterial genes, along with root-derived LMWOAs, were profiled using amplicon sequencing and non-targeted metabolomics. The mechanisms underlying the stimulation of P-mobilizing bacteria for soil P mobilization and plant P uptake were investigated through in vitro and pot experiments, complemented by transcriptomics and proteomics. Field data indicated that manure amendment increased the soil labile-P fraction and P bioavailability. Additionally, it was observed that root-derived aliphatic and aromatic LMWOAs modulated the structure, diversity, and abundance of pqqC and phoD genes, correlating with the expression levels of phosphate transporters and acid phosphatases in maize roots. In vitro and pot experiments validated the effects of 2-hydroxycinnamic, syringic, isoferulic, and alpha-ketoglutaric acids on the keystone bacteria (Burkholderia, Pseudomonas, Mesorhizobium, and Sinorhizobium). These molecules enhanced the diversity and abundance of pqqC and phoD genes, affecting maize root morphology, plant gene expression, and protein synthesis. This study elucidated the intricate interactions between maize root exudates and P-mobilizing bacteria. The results provide new avenues for exploring root-derived LMWOAs as signaling molecules to optimize synthetic biological strategies for sustainable agriculture.