With the death and decomposition of widely distributed photosynthetic organisms, free natural pigments are often detected in surface water, sediment and soil. Whether free pigments can act as photosensitizers to drive biophotoelectrochemical metabolism in nonphotosynthetic microorganisms has not been reported. In this work, we provide direct evidence for the photoelectrophic relationship between extracellular chlorophyll a (Chl a) and nonphotosynthetic microorganisms. The results show that 10 μg of Chl a can produce significant photoelectrons (∼0.34 A/cm2) upon irradiation to drive nitrate reduction in Shewanella oneidensis. Chl a undergoes structural changes during the photoelectric process, thus the ability of Chl a to generate a photocurrent decreases gradually with increasing illumination time. These changes are greater in the presence of microorganisms than in the absence of microorganisms. Photoelectron transport from Chl a to S. oneidensis occurs through a direct pathway involving the cytochromes MtrA, MtrB, MtrC and CymA but not through an indirect pathway involving riboflavin. These findings reveal a novel photoelectrotrophic linkage between natural photosynthetic pigments and nonphototrophic microorganisms, which has important implications for the biogeochemical cycle of nitrogen in various natural environments where Chl a is distributed.

Nitrogen fixation by the diazotrophic cyanobacterium Trichodesmium contributes up to 50% of the bioavailable nitrogen in the ocean. N2 fixation by Trichodesmium is limited by the availability of nutrients, such as iron (Fe) and phosphorus (P). Although colloids are ubiquitous in the ocean, the effects of Fe limitation on nitrogen fixation by marine colloids (MC) and the related mechanisms are largely unexplored. In this study, we found that MC exhibit photoelectrochemical properties that boost nitrogen fixation by photoelectrophy in Trichodesmium erythraeum. MC efficiently promote photosynthesis in T. erythraeum, thus enhancing its growth. Photoexcited electrons from MC are directly transferred to the photosynthetic electron transport chain and contribute to nitrogen fixation and ammonia assimilation. Transcriptomic analysis revealed that MC significantly upregulates genes related to the electron transport chain, photosystem, and photosynthesis, which is consistent with elevated photosynthetic capacities (e.g., Fv/Fm and carboxysomes). As a result, MC increase the N2 fixation rate by 67.5-89.3%. Our findings highlight a proof-of-concept electron transfer pathway by which MC boost nitrogen fixation, broadening our knowledge on the role of ubiquitous colloids in marine nitrogen biogeochemistry.

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.