Genome-Resolved Metagenomics and Metatranscriptomics Reveal that Aquificae Dominates Arsenate Reduction in Tengchong Geothermal Springs

Elevated arsenic (As) is common in geothermal springs, shaping the evolution of As metabolism genes and As transforming microbes. Herein, genome-level microbial metabolisms and As cycling strategies in Tengchong geothermal springs were demonstrated for the first time based on metagenomic and metatranscriptomic analyses. Sulfur cycling was dominated by Aquificae oxidizing thiosulfate via the sox system, fueling the respiration and carbon dioxide fixation processes. Arsenate reduction via arsC [488.63 ± 271.60 transcripts per million (TPM)] and arsenite efflux via arsB (442.98 ± 284.81 TPM) were the primary detoxification pathway, with most genes and transcripts contributed by the members in phylum Aquificae. A complete arsenotrophic cycle was also transcriptionally active as evidenced by the detection of aioA transcripts and arrA transcript reads mapped onto metagenome-assembled genomes (MAGs) affiliated with Crenarchaeota. MAGs affiliated with Aquificae had great potential of reducing arsenate via arsC and fixing nitrogen and carbon dioxide via nifDHK and reductive tricarboxylic acid (rTCA) cycle, respectively. Aquificae's arsenate reduction potential via arsC was observed for the first time at the transcriptional level. This study expands the diversity of the arsC-based arsenate-reducing community and highlights the importance of Aquificae to As biogeochemistry.