Electric syntrophy-driven modulation of Fe0-dependent microbial denitrification

Abstract

In natural or engineered anaerobic environments, iron oxidation-driven microbial denitrification plays a critical role in the water or wastewater treatment. Herein, we report a previously unidentified metallic iron (Fe⁰)-dependent denitrification mode driven by the electro-syntrophic interaction between electroactive microorganism and denitrifier. In a model denitrifying consortium of Shewanella oneidensis and Pseudomonas aeruginosa, we find that P. aeruginosa can accept electrons for nitrate reduction via the constructed electron transfer system of Fe⁰–S. oneidensis–P. aeruginosa. In the electro-syntrophic consortium, the membrane-bound CymA–OmcA–MtrC protein complexes of S. oneidensis drive the generation, transfer and consumption of electrons, thus enabling modulation of microbial metabolic activity. Specially, using Fe⁰ as the sole electron donor, S. oneidensis can act as a bio-engine to harvest electrons and conserve energy from Fe⁰ biocorrosion. Electrons released by S. oneidensis are utilized by P. aeruginosa for accomplishing microbial denitrification. Metatranscriptomics analysis demonstrated that the direct electron cross-feeding process facilitates the expression of genes encoding for denitrification enzymes, intracellular electron transfer proteins, and quorum sensing of P. aeruginosa. The Fe⁰-dependent electronic syntrophy in this work could provide a metabolic window for the growth of denitrifiers that is a new insight into nitrate removal or global nitrogen cycle.