Biological sulfur oxidation mediated arsenate reduction, a key process in arsenic-contaminated habitats

Arsenate reduction is a major cause of As release from soils which threatens more than 200 million people worldwide. While heterotrophic As(V) reduction has been extensively investigated, the mechanism of chemolithotrophic As(V) reduction is less studied. Since As is frequently found as sulfidic minerals in the environment, microbial-mediated sulfur oxidation coupled to As(V) reduction (SOAsR), a chemolithotrophic process, may be more favorable in oligotrophic mining-impacted sites (e.g., As-contaminated mine tailings). While SOAsR is thermodynamically favorable, knowledge regarding this biogeochemical process is still limited. The current study suggested that SOAsR was a more dominant process compared to heterotrophic As(V) reduction in oligotrophic sites, such as mine tailings. A combination of DNA-SIP and metagenome binning revealed members of the genera Sulfuricella, Ramlibacter, and Sulfuritalea as SOAsRBs in mine tailings. Genome mining further expanded the list of SOAsRBs to diverse phylogenetic lineages such as members associated with Burkholderiaceae and Desulfuribacteraceae. Meta-analysis using multiple tailing sample metagenomes across southern China confirmed that the putative SOAsRB were the dominant As(V) reducers in these sites. Together, the current findings expand our knowledge regarding the chemolithotrophic As(V) reduction process, which may be harnessed to facilitate future remediation practices in mine tailings.

砷酸盐还原是土壤中砷释放的主要诱因，该过程威胁着全球超过2亿人口的健康。尽管异养型五价砷（As(V)）还原已被广泛研究，但化能自养型五价砷还原的机制仍有待深入阐释。由于砷在环境中常以硫化物矿物形式存在，微生物介导的硫氧化耦合五价砷还原（sulfur oxidation coupled to As(V) reduction, 缩写SOAsR）作为一种化能自养过程，在贫营养且受采矿活动影响的生境（如受砷污染的矿山尾矿）中更具生存优势。尽管SOAsR在热力学上具备可行性，但目前学界对这一生物地球化学过程的认知仍较为有限。本研究表明，在矿山尾矿这类贫营养生境中，SOAsR相较于异养型五价砷还原是更为主导的过程。通过DNA稳定性同位素探针（DNA-SIP）与宏基因组分箱（metagenome binning）的联合分析，研究人员在矿山尾矿中鉴定出Sulfuricella、Ramlibacter及Sulfuritalea菌属的类群为SOAsR功能菌（SOAsRBs）。基因组挖掘进一步将SOAsR功能菌的类群拓展至多个系统发育分支，例如伯克霍尔德菌科（Burkholderiaceae）与脱硫杆菌科（Desulfuribacteraceae）的相关成员。对中国南方多地多份尾矿样本宏基因组开展的元分析证实，推定的SOAsR功能菌是这些生境中占主导的五价砷还原菌。综上，本研究的发现拓展了学界对化能自养型五价砷还原过程的认知，该过程有望被应用于未来矿山尾矿的修复实践。