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

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.