Indicator species drive the key ecological functions of microbiota in a river impacted by acid mine drainage generated by rare earth elements mining in South China

Acid mine drainage (AMD) generated by rare earth elements (REEs) deposits exploration contains high concentrations of REEs, ammonium and sulfates, which is quite different from typical metallic AMD. Currently, microbial responses and ecological functions in REEs-AMD impacted rivers are unknown. Here, 16S rRNA analysis and genome-resolved metagenomics were performed on microbial community collected from a REEs-AMD contaminated river. The results showed that REEs-AMD significantly changed river microbial diversity and shaped unique indicator species (e.g. Thaumarchaeota, Methylophilales, Rhodospirillales and Burkholderiales). The main environmental factors regulating community were pH, ammonium and REEs, among which high concentration of REEs increased REEs-dependent enzyme-encoding genes (XoxF and ExaF/PedH). Additionally, we reconstructed 566 metagenome-assembled genomes covering 70.4% of identifying indicators. Genome-centric analysis revealed that the abundant archaea Thaumarchaeota and Xanthomonadaceae were often involved in nitrification and denitrification, while family Burkholderiaceae were capable of sulfide oxidation coupled with dissimilatory nitrate reduction to ammonium. These indicators play crucial roles in nitrogen and sulfur cycling as well as REEs immobilization in REEs-AMD contaminated rivers. This study confirmed the potential dual effect of REEs on microbial community at the functional gene level. Our investigation on the ecological roles of indicators further provided new insights for the development of REEs-AMD bioremediation.