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The use of plant growth-promoting rhizobacteria (PGPR) for the bioremediation of heavy metal cadmium (Cd) and for enhancing plant growth in Cd-polluted soil is widely recognized as an effective approach. This study aimed to isolate Cd-resistant bacteria with plant growth-promoting (PGP) traits from the rhizosphere of vegetables subjected to metal contamination and to investigate the mechanisms associated with Cd adsorption as well as its impact on Cd uptake in lettuce. Six Cd-resistant bacterial strains were isolated from rhizosphere soil, among which the R27 strain exhibited the highest tolerance to Cd (minimum inhibitory concentration of 2000 mg/L) along with PGP traits, including phosphate solubilization (385.11 mg/L), the production of indole-3-acetic acid (IAA) (35.92 mg/L), and siderophore production (3.34 mg/L). Through a range of physiological, biochemical, and molecular assessments, the R27 strain was classified as Bacillus siamensis. This strain demonstrated notable efficiency in removing Cd2+ from the growth medium, achieving an efficacy of 80.1%. This removal was facilitated by cell surface adsorption through functional groups such as O–H, C=O, –CO–NH–, and C–O, alongside intracellular Cd accumulation, as evidenced by SEM, TEM, EDX, and FTIR analyses. Pot culture experiments indicated that R27 significantly promoted lettuce seedling growth and helped plants tolerate Cd stress, with the underlying mechanisms likely involving increased antioxidant activities for scavenging reactive oxygen species (ROS) induced by Cd stress, and reduced Cd2+ levels in lettuce seedlings to mitigate Cd2+ toxicity. These physiological changes were further supported by the down-regulation of genes associated with cadmium transport, including IRT1, Nramp1, HMA2, HMA4, ZIP4, and ZIP12, as well as the significantly reduced root bio-concentration factor (BCF) and translocation factor (TF). In summary, the R27 strain offers considerable potential in the bioremediation of Cd-polluted soils and can serve as a bio-fertilizer to enhance plant growth. [ABSTRACT FROM AUTHOR]