Genome-resolved metagenomics of an autotrophic thiocyanate-remediating microbial bioreactor consortium

Industrial thiocyanate (SCN^-) waste streams from gold mining and coal coking have polluted environments worldwide. Modern SCN^- bioremediation involves use of complex engineered heterotrophic microbiomes; little attention has been given to the ability of a simple environmental autotrophic microbiome to biodegrade SCN^-. Here we present results from a bioreactor experiment inoculated with SCN^- -loaded mine tailings, incubated autotrophically, and subjected to a range of environmentally relevant conditions. Genome-resolved metagenomics revealed that SCN^- hydrolase-encoding, sulphur-oxidizing autotrophic bacteria mediated SCN^- degradation. These microbes supported metabolically-dependent non-SCN^--degrading sulphur-oxidizing autotrophs and non-sulphur oxidizing heterotrophs, and "niche" microbiomes developed spatially (planktonic versus sessile) and temporally (across changing environmental parameters). Bioreactor microbiome structures changed significantly with increasing temperature, shifting from Thiobacilli to a novel SCN^- hydrolase-encoding gammaproteobacteria. Transformation of carbonyl sulphide (COS), a key intermediate in global biogeochemical sulphur cycling, was mediated by plasmid-hosted CS₂ and COS hydrolase genes associated with Thiobacillus, revealing a potential for horizontal transfer of this function. Our work shows that simple native autotrophic microbiomes from mine tailings can be employed for SCN^- bioremediation, thus improving the recycling of ore processing waters and reducing the hydrological footprint of mining.