Conventional biodecolorization of azo dyes is often limited by the lack of sustainable and bioavailable electron donors in aqueous environments. This limitation may be overcome by light-excited photoelectrons that drive the microbial reduction of azo dyes. Here, we innovatively developed a surface-precipitated Geobacter sulfurreducens− CdS biohybrid for the bioreduction of methyl orange (MO), a typical azo dye, driven by light. This biohybrid system exhibited the maximum kinetic constant at 1.441 h −1 , which is, to the best of our knowledge, the highest value reported thus far for MO biodecolorization. The intermittent illumination results indicated that G. sulfurreducens could directly use extracellular photoelectrons (rather than electrons from organics oxidization by strains) in order to perform decolorization on the bacterial cell surface. This can be attributed to the direct electron transfer from CdS nanoparticles to G. sulfurreducens. In addition, OmcB was identified as a key outermembrane protein that may act as a capacitor to modulate electron transfer from CdS to MO. This biohybrid catalytic approach may serve as a new strategy for azo dye degradation in oligotrophic surface waters and can deepen our knowledge on interactions between light, semiconductors and micro-organisms.

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 Mn 3 O 4 nanozyme-coated biosemiconductor, Thiobacillus denitrificans-cadmium sulfide (T. denitrificans-CdS@Mn 3 O 4 ), via a simple, fast, and economic method. After Mn 3 O 4 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@Mn 3 O 4 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 Mn 3 O 4 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 Mn 3 O 4 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 Mn 3 O 4 . 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.

Diazotrophs can produce bioavailable nitrogen from inert N2 gas by bioelectrochemical nitrogen fixation (e-BNF), which is emerging as an energy-saving and highly selective strategy for agriculture and industry. However, current e-BNF technology is impeded by requirements for NH4+-assimilation inhibitors to facilitate intracellular ammonia secretion and precious metal catalysts to generate H2 as the energy-carrying intermediate. Herein, we initially demonstrate inhibitor- and catalyst-less extracellular NH4+ production by the diazotroph Pseudomonas stutzeri A1501 using an electrode as the sole electron donor. Multiple lines of evidence revealed that P. stutzeri produced 2.32±0.25 mg/L of extracellular NH4+ at a poised potential of -0.3 V (vs. standard hydrogen electrode (SHE)) without the addition of inhibitors or expensive catalysts. The electron uptake mechanism was attributed to the endogenous electron shuttle phenazine-1-carboxylic acid, which was excreted by P. stutzeri and mediated electron transfer from electrodes into cells to directly drive N2 fixation. The faradaic efficiency was 20%±3% which was 2-4 times that of previous e-BNF using the H2-mediated pathway. This study reports a diazotroph capable of producing secretable NH4+ via extracellular electron uptake, which has important implications for optimizing the performance of e-BNF systems and exploring the novel nitrogen-fixing mode of syntrophic microbial communities in the natural environment. IMPORTANCE Ammonia greatly affects the global ecology, agriculture and the food industry. Diazotrophs with an enhanced capacity of extracellular NH4+ excretion have been proven to be more beneficial to the growth of microalgae and plants, whereas most previously reported diazotrophs produce intracellular organic nitrogen in the absence of chemical suppression and genetic manipulation. Here, we demonstrate that Pseudomonas stutzeri A1501 is capable of extracellular NH4+ production without chemical suppression or genetic manipulation when the extracellular electrode is used as the sole electron donor. We also reveal the electron uptake pathway from the extracellular electron-donating partner to P. stutzeri A1501 via redox electron shuttle phenazines. Since both P. stutzeri A1501 and potential electron-donating partners (such as electroactive microbes and natural semiconductor minerals) are abundant in diverse soils and sediments, P. stutzeri A1501 has broader implications on the improvement of nitrogen fertilization in the natural environment.

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.

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.