Anthraquinone-2-Sulfonate as a Microbial Photosensitizer and Capacitor Drives Solar-to-N2O Production with a Quantum Efficiency of Almost Unity.

Semiartificial photosynthesis shows great potential in solar energy conversion and environmental application. However, the rate-limiting step of photoelectron transfer at the biomaterial interface results in an unsatisfactory quantum yield (QY, typically lower than 3%). Here, an anthraquinone molecule, which has dual roles of microbial photosensitizer and capacitor, was demonstrated to negotiate the interface photoelectron transfer via decoupling the photochemical reaction with a microbial dark reaction. In a model system, anthraquinone-2-sulfonate (AQS)-photosensitized Thiobacillus denitrificans, a maximum QY of solar-to-nitrous oxide (N2O) of 96.2% was achieved, which is the highest among the semiartificial photosynthesis systems. Moreover, the conversion of nitrate into N2O was almost 100%, indicating the excellent selectivity in nitrate reduction. The capacitive property of AQS resulted in 82-89% of photoelectrons released at dark and enhanced 5.6-9.4 times the conversion of solar-to-N2O. Kinetics investigation revealed a zero-order- and first-order- reaction kinetics of N2O production in the dark (reductive AQS-mediated electron transfer) and under light (direct photoelectron transfer), respectively. This work is the first study to demonstrate the role of AQS in photosensitizing a microorganism and provides a simple and highly selective approach to produce N2O from nitrate-polluted wastewater and a strategy for the efficient conversion of solar-to-chemical by a semiartificial photosynthesis system.

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.

Mn3O4 Nanozyme Coating Accelerates Nitrate Reduction and Decreases N2O Emission during Photoelectrotrophic Denitrification by Thiobacillus denitrificans-CdS.

Biosemiconductors are highly efficient systems for converting solar energy into chemical energy. However, the inevitable presence of reactive oxygen species (ROS) seriously deteriorates the biosemiconductor performance. This work successfully constructed a Mn3O4 nanozyme-coated biosemiconductor, Thiobacillus denitrificans-cadmium sulfide (T. denitrificans-CdS@Mn3O4), via a simple, fast, and economic method. After Mn3O4 coating, the ROS were greatly eliminated; the concentrations of hydroxyl radicals, superoxide radicals, and hydrogen peroxide were reduced by 90%, 77.6%, and 26%, respectively, during photoelectrotrophic denitrification (PEDeN). T. denitrificans-CdS@Mn3O4 showed a 28% higher rate of nitrate reduction and 78% lower emission of nitrous oxide (at 68 h) than that of T. denitrificans-CdS. Moreover, the Mn3O4 coating effectively maintained the microbial viability and photochemical activity of CdS in the biosemiconductor. Importantly, no lag period was observed during PEDeN, suggesting that the Mn3O4 coating does not affect the metabolism of T. denitrificans-CdS. Immediate decomposition and physical separation are the two possible ways to protect a biosemiconductor from ROS damage by Mn3O4. This study provides a simple method for protecting biosemiconductors from the toxicity of inevitably generated ROS and will help develop more stable and efficient biosemiconductors in the future.