Identification of autotrophic bacteria mediate Cr(VI) reduction coupled with sulfur oxidation in oligotrophic soils

Chromium (Cr) is the second most common metal contaminant in ground water, soil, and sediments. Hexavalent chromium (Cr(VI)) reduction is crucial for alleviating its toxicity and thus is of environmental importance. In nutrient-rich soil, Cr(VI) reduction can be driven by heterotrophic bacteria utilizing organic matters as electron donors, which might be restrained due to the limited organic matters. In oligotrophic habitats, microorganisms may alternatively use inorganic compounds as electron donor to drive Cr(VI) reduction. However, autotrophic Cr(VI) reduction using inorganic compounds was not reported yet. In this study, enrichment cultures were established with the nutrient-limited soil from the tailing to investigate the autotrophic Cr(VI) reduction using reduced S as electron donor. Our findings revealed that the S-oxidizing Cr(VI) reduction (i.e., SOCrR) driven by autotrophic bacteria indeed existed in the oligotrophic soil. DNA-stable isotope probing (SIP) combined with metagenomics identified that the Intrasporangiaceae was the putative autotrophic Cr(VI) reducer utilizing S as the electron donor (i.e., SOCrRB). Genes associated with Cr(VI) reduction (i.e., chrR, qor, and oye), S oxidation (i.e., dsr and sqr) and Wood-Ljungdahl pathway were also observed in the Intrasporangiaceae-affiliated metagenome-assembled genomes (MAGs), thereby supporting their role in autotrophic SOCrR. In addition, pangenomic analysis demonstrated the capacity of SOCrR in Intrasporangiaceae-associated bacteria was widespread in various environments. These findings expanded our knowledge of the Cr(VI) reduction and provided a novel guidance for management and bioremediation of Cr pollution, especially in the nutrient-limited environment.