Understanding the microbial communities involved in the global sulfur cycle is crucial for comprehending key biogeochemical processes on Earth. Most studies, however, are biased towards the marine ecosystems, as terrestrial sulfur cycle rarely investigated. In this study, we employed culture-dependent techniques and metagenomics to investigate functional, taxonomic and culturable of sulfur-cycling bacteria in extremely contaminated soils. Our findings reveal that elevated concentrations of xenobiotic pollutants, bulk sulfur content, and fluctuating redox conditions have shaped a unique microbial community involved in sulfur transformation. This community comprises non-canonical taxa carrying out typical reactions (e.g., sulfate-reducing acidobacteria), known taxa engaged in various oxidative, reductive, and organosulfur transformations (e.g., sulfur oxidizing alpha-, gamma-, and betaproteobacteria), as well as previously unidentified taxa that remain uncultured and may possess novel genes related to sulfur compound metabolism. Additionally, multiple taxa contribute to the replenishment of readily consumable compounds like sulfite and thiosulfate, facilitating cryptic biogeochemical cycling of molecules with high turnover rates but low absolute abundance. Our analysis also supports the idea that known sulfate-reducing bacteria behave differently in soils compared to aquatic habitats and belong to the soil rare biosphere, still greatly affecting their ecosystem.