Dissolved Organic Matter Acting as a Microbial Photosensitizer Drives Photoelectrotrophic Denitrification

The biogeochemical fates of dissolved organic matter (DOM) show important environmental significance in aqueous ecosystems. However, the current understanding of the trophic relationship between DOM and microorganisms limits the ability of DOM to serve as a heterotrophic substrate or electron shuttle for microorganisms. In this work, we provide the first evidence of photoelectrophy, a new trophic linkage, that occurs between DOM and nonphototrophic microorganisms. Specifically, the photoelectrotrophic denitrification process was demonstrated in a Thiobacillus denitrificans-DOM coupled system, in which DOM acted as a microbial photosensitizer to drive the model denitrifier nitrate reduction. The reduction of nitrate followed a pseudo-first-order reaction with a kinetic constant of 0.06 ± 0.003 h^-1, and the dominant nitrogenous product was nitrogen. The significant upregulated (p < 0.01) expression of denitrifying genes, including nar, nir, nor, and nos, supported that the conversion of nitrate to nitrogen was the microorganism-mediated process. Interestingly, the photoelectrophic process triggered by DOM photosensitization promotes humification of DOM itself, an almost opposite trend of pure DOM irradiation. The finding not only reveals a so far overlooked role of DOM serving as the microbial photosensitizer in sunlit aqueous ecosystems but also suggests a strategy for promoting sunlight-driven denitrification in surface environments.