AQDS Activates Extracellular Synergistic Biodetoxification of Copper and Selenite via Altering the Coordination Environment of Outer-Membrane Proteins

The biotransformation of heavy metals in the environment is usually affected by co-existing pollutants like selenium (Se), which may lower the ecotoxicity of heavy metals, but the underlying mechanisms remain unclear. Here, we shed light on the pathways of copper (Cu2+) and selenite (SeO32-) synergistic biodetoxification by Shewanella oneidensis MR-1 and illustrate how such processes are affected by anthraquinone-2,6-disulfonate (AQDS), an analogue of humic substances. We observed the formation of copper selenide nanoparticles (Cu2-xSe) from synergistic detoxification of Cu2+ and SeO32- in the periplasm. Interestingly, adding AQDS triggered a fundamental transition from periplasmic to extracellular reaction, enabling 14.7-fold faster Cu2+ biodetoxification (via mediated electron transfer) and 11.4-fold faster SeO32- detoxification (via direct electron transfer). This is mainly attributed to the slightly raised redox potential of the heme center of AQDS-coordinated outer-membrane proteins that accelerates electron efflux from the cells. Our work offers a fundamental understanding of the synergistic detoxification of heavy metals and Se in a complicated environmental matrix and unveils an unexpected role of AQDS beyond electron mediation, which may guide the development of more efficient environmental remediation and resource recovery biotechnologies.

Automated summary

This study reveals the synergistic detoxification of Cu2+ and SeO32- by Shewanella oneidensis MR-1 in a complex environmental matrix. The addition of AQDS triggers a transition from intracellular to extracellular reaction, accelerating Cu2+ and SeO32- biodetoxification. The slightly raised redox potential of AQDS-coordinated outer-membrane proteins contributes to the faster electron efflux from the cells.