Iron-reduction driven extracellular electron transfer widely promotes microbial reductive dechlorination metabolism

Abstract

Biological iron reduction and reductive dehalogenation occur in similar ecological environments, however, how Fe(III)/Fe(II) redox cycles impact the microbial dehalogenation processes remains controversial. In this study, the favorable microbial reductive dechlorination activity has been widely observed in iron-rich river sediments by national sampling, with the dechlorination efficiency showing a positive correlation with the concentration of Fe(III). Microcosm experiments demonstrated that the addition of nano-hematite resulted in a maximum increase of 2.16 times in the dechlorination rate constant (k) for 2,4,6-trichlorophenol, achieved via synergistic interactions with Fe(III) reduction. Multi-tools, including transcriptomic analyses, revealed that the addition of nano-hematite enhanced the process of Fe(III) reduction by upregulating genes associated with extracellular electron transfer (e.g., CYC, pliM) and conductive biofilm formation (e.g., livH, secY, wza). This synergistic Fe(III) reduction further facilitated intracellular carbon metabolism, energy production, and reductive dechlorination, as confirmed by the upregulated functional genes identified through transcriptomics and RT-qPCR. The discovery of the novel phenomenon involving synergistic Fe(III) reduction and dehalogenation broadens our understanding of the biochemical cycling of organohalides (e.g., chlorinated phenols) in iron-rich environment, and provides a feasible strategy for improving biodehalogenation through the regulation of carbon and electron flow at sites contaminated with organohalides.