Environmental microbes in rhizosphere soil and surrounding plants have the potential to alter ecosystem functions. We investigated the microbial communities inhabiting the rhizosphere soils of both serpentine and non-serpentine rhizosphere zones to evaluate their heavy metal tolerance and ability to promote plant growth, utilizing 16S rRNA metabarcoding. The Biolog-EcoPlate technique was employed to determine how abiotic stress factors affect carbon utilization capacity by rhizospheric microbial communities in the serpentine geo-ecosystem. The phyla Proteobacteria, Acidobacteria, Bacteroidetes, and Nitrospirae colonized in the roots of Miscanthus sp., Biden sp., and Oryza sp. showed noticeable differences in different rhizosphere zones. The PICRUSt2-based analysis identified chromium/iron resistance genes (ceuE, chrA) and arsenic resistance genes (arsR, acr3, arsC) abundant in all the studied rhizosphere soils. Notably, nickel resistance genes (nikA, nikD, nikE, and nikR) from Arthrobacter, Microbacterium, and Streptomyces strongly correlate with functions related to solubilization of nickel and an increase in siderophore and IAA production. The abundance of Arthrobacter, Clostridium, Geobacter, Dechloromonas, Pseudomonas, and Flavobacterium was positively correlated with chromium and nickel but negatively correlated with the calcium/magnesium ratio. Our results contribute to a better understanding of the functions of plant-tolerant PGPR interaction in the heavy metal-contaminated rhizosphere and eco-physiological responses from long-term biological weathering.