Novel Photoelectron-Assisted Microbial Reduction of Arsenate Driven by Photosensitive Dissolved Organic Matter in Mine Stream Sediments

Abstract

The microbial reduction of arsenate (As(V)) significantly contributes to arsenic migration in mine stream sediment, primarily driven by heterotrophic microorganisms using dissolved organic matter (DOM) as a carbon source. This study reveals a novel reduction pathway in sediments that photosensitive DOM generates photoelectrons to stimulate diverse nonphototrophic microorganisms to reduce As(V). This microbial photoelectrophic As(V) reduction (PEAsR) was investigated using microcosm incubation, which showed the transfer of photoelectrons from DOM to indigenous sediment microorganisms, thereby leading to a 50% higher microbial reduction rate of As(V). The abundance of two marker genes for As(V) reduction, arrA and arsC, increased substantially, confirming the microbial nature of PEAsR rather than a photoelectrochemical process. Photoelectron ion is unlikely to stimulate photolithoautotrophic growth. Instead, diverse nonphototrophic genera, e.g., Cupriavidus, Sphingopyxis, Mycobacterium, and Bradyrhizobium, spanning 13 orders became enriched by 10–50 folds. Metagenomic binning revealed their genetic potential to mediate the photoelectron-assisted reduction of As(V). These microorganisms contain essential genes involved in respiratory As(V) reduction, detoxification As(V) reduction, dimethyl sulfoxide reductase family, c-type cytochromes, and multiple heavy-metal resistance but lack a complete photosynthesis system. The novel microbial PEAsR pathway offers new insights into the interaction between photoelectron utilization and nonphototrophic As(V)-reducing microorganisms, which may have profound implications for arsenic pollution transportation in mine stream sediment.