Thiocyanate (SCN-) pollution from mining and coking presents a problem worldwide. Here we experimentally investigated the capacity of an autotrophic microbiome sourced from mine tailings to degrade SCN-. A bioreactor was inoculated with tailings, incubated autotrophically, and subjected to a range of environmental conditions. Genome-resolved metagenomics revealed that SCN-hydrolase-encoding, sulphur-oxidizing autotrophic bacteria controlled SCN-degradation. These bacteria supported metabolically-dependent non-SCN--degrading sulphur-oxidizing autotrophs and non-sulphur oxidising heterotrophs. Microbiome structures varied spatially (planktonic versus sessile) and temporally (across changing environmental conditions), and shifted from Thiobacilli to novel gammaproteobacteria. Degradation of carbonyl sulphide (COS), a key intermediate in the global biogeochemical sulphur cycle, was attributed to plasmid-hosted CS2and COS hydrolase genes associated withThiobacillus, revealing the possibility for lateral transfer of this capability. In summary, we show that native autotrophic microbiomes from mine tailings can be employed for SCN-bioremediation, thus reducing the hydrological impact of mining.