Insights into the hydrogen-fueled bioreduction of vanadium(V) by marine Shewanella sp. FDA-1: Process and mechanism

Abstract

Microbial-driven V(V) reduction plays a crucial role in its biogeochemical cycle, yet the mechanisms underlying this bioreduction remain inadequately understood. While the effectiveness of organic compounds as electron donors in facilitating bacterial reduction of V(V) has been established, the role of inorganic electron donors in initiating this process at the level of pure cultured bacteria has not been explored. In this study, we report on a marine Shewanella sp. FDA-1 that utilizes hydrogen (H2) as an energy source to reduce V(V). In addition, the reduction mechanism was investigated through a combination of genomics, RT-qPCR, heterologous expression of key proteins, extracellular secretion analyses, and electron transfer activity assays. Our results demonstrate that H2 serves as an effective electron donor, enabling Shewanella sp. FDA-1 to reduce V(V) across various salinities (2–7 %) and pH values (5−9). When exposed to 5 mM V(V), the presence of 1–20 mL of H2 resulted in V(V) bioreduction rates ranging from 0.039 to 0.11 h−1 (R2 > 0.73). Amorphous V(IV) compounds were characterized as reduction products using XRD, XPS, FTIR, and SEM. Mechanistic studies indicate that the glutathione system, cytochromes, and extracellular substances such as riboflavin play important roles in V(V) reduction (p < 0.05). Furthermore, our findings reveal that the addition of H2 and lactate triggers different response sequences among these three reduction pathways, suggesting distinct reduction mechanisms between organic and inorganic electron donors. These insights enhance our understanding of microbial vanadium transformation and provide valuable guidance for developing novel H2-based remediation technologies for vanadium-contaminated environments.