Plant growth-promoting bacteria reshape rhizosphere microecology to regulate Cd, Pb, and Zn mobilization at root-soil interface

Abstract

Heavy metal (HM) contamination poses an escalating threat to human health and global terrestrial ecosystems. Inexpensive, eco-friendly technologies that reduce HM concentrations in soil are needed. Utilizing the synergy between hyperaccumulating plants and their rhizosphere microbes offers a promising approach to the bioremediation of HM-contaminated sites; however, the mechanisms underlying this plant-microbe relationship remain unclear. In the present study, high-resolution in situ imaging revealed that inoculation of the plant growth-promoting bacterium (PGPB) Bacillus megaterium altered the rhizosphere microenvironment of the Cd and Mn-hyperaccumulator Celosia argentea grown in HM-contaminated field soil. Decreased pH, increased O₂ fluxes, and stimulated microbial activity and enzyme-mediated C and P cycling were observed. Multi-omics analyses suggested that PGPB-modulated rhizosphere microbial succession selectively enriched beneficial taxa and functional genes associated with nutrient cycling and metal resistance. Transcriptomic and metabolomic profiling analysis revealed that the PGPB induced transcriptional reprogramming in C. argentea, leading to the activation of antioxidant defenses, metal transporter expression, and root exudate metabolism, with a focus on lipid- and sphingolipid-related pathways. These processes collectively enhanced the mobilization and uptake of Cd, Pb, and Zn at the root-soil interface, suggesting that the mutualistic plant-microbe system facilitated HM phytoextraction efficiency. Our findings offer novel insights into how microbial inoculants can rewire the rhizosphere microecology to regulate metal dynamics and enhance the remediation of multi-metal-contaminated soils.