Phosphate-solubilizing inoculants induce stage-specific rhizosphere microbiome shifts and enhance chickpea symbiosis under low P availability

Understanding legume symbiotic efficiency in response to phosphate (P) solubilizing microbes (PSM) is crucial, given their ability to synergize with rhizobial strains and promote rhizosphere interactions that enhance soil P availability and legume nodulation. However, the mechanistic understanding deciphering how PSM likely to influence legume symbiotic efficiency, including rhizosphere microbial dynamics, remains not well known. This study assessed the ability of twenty-four PSM (bacteria “PSB” and fungi “PSF”) to induce chickpea nodulation and identified key rhizosphere traits through which PSM may enhance chickpea symbiotic performance under low P availability. Results demonstrated that only five PSM inoculants enhanced symbiotic traits of Mesorhizobium-inoculated chickpea, including nodule biomass, leghemoglobin content, intra-tissular P (Pi), and acid phosphatase (APase) activity, as well as plant biomass and nutrient uptake at both flowering and reproductive growth stages. Notably, PSM consortia significantly outperformed single inoculants by strengthening the link between above- and below-ground plant traits. This was supported by strong positive correlations between nodule Pi content and both nodule APase activity (R = 0.94**, p ≤ 0.01) and leghemoglobin content (R = 0.95**, p ≤ 0.01). The rhizosphere P-related traits, including P availability, rhizosphere and root APase activity, root Pi content, and shoot P uptake were significantly higher than in uninoculated treatments. These responses were concomitant with specific modifications in rhizosphere microbial communities that were significantly correlated with chickpea symbiotic traits and overall growth parameters. At the flowering stage, bacterial community composition favored beneficial N2-fixing taxa (Acetobactereaceae, Beijerinckiaceae, Rhizobiales), with Mesorhizobium showing strong correlations with plant growth traits. At the reproductive stage, the fungal community was enriched in disease-suppressive genera (Trichoderma and Talaromyces). Our findings reveal a stage-specific microbial cooperation that enhances symbiotic performance, plant growth, and nutrient uptake in chickpea under low P availability.