Bacteria-driven copper redox reaction coupled electron transfer from Cr(VI) to Cr(III): A new and alternate mechanism of Cr(VI) bioreduction

Cr(VI) released into the environment inevitably co-exists with other contaminants, such as heavy metal ions, thus altering the performance of bacteria for Cr(VI) reduction; however, the mechanism underlying Cr(VI)-reducing bacterial response to heavy metal ions remains elusive. Herein, we investigate the toxic effects of Cu(II) and Cr(VI) on Cr(VI)-reducing bacterium Pannonibacter phragmitetus D-6 (hereafter D-6), which changes the primary metabolic pattern of Cr(VI). At Cu(II) concentrations of 10-100 mg/L, the efficiency of Cr(VI) reduction increases significantly. The co-exposure of Cr(VI) and Cu(II) induces D-6 to preferentially respond to Cu(II) through electrostatic forces, which is then reduced to Cu(I) outside and inside the bacterial cells. The original pathways for Cr(VI) reduction are weakened via downregulating genes related to Cr(VI) transport and reduction. A new mechanism involving Cu(II)-mediated electron transfer from D-6 to Cr(VI) is elucidated. Specially, Cu(II) accumulates around the cells as an electron shuttle and promotes Cr(VI) reduction. Genes encoding cytochromes involved in electron transfer are significantly up-regulated, thus promoting Cu(II) reduction. The Cu(II)/Cu(I) redox cycle ensures the continuous bioremoval of Cr(VI) in a cycle test. This study reveals an overlooked mechanism for Cr(VI) reduction, which provides theoretical guidance for designing practical microbial process to remediate Cr(VI) contamination.