Scalable Ammonia Synthesis in Fermentors Using Quantum Dot-Azotobacter vinelandii Hybrids

doi:10.21203/rs.3.rs-4122105/v1

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Scalable Ammonia Synthesis in Fermentors Using Quantum Dot-Azotobacter vinelandii Hybrids

https://doi.org/10.21203/rs.3.rs-4122105/v1

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published 13 Aug, 2024

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This study introduces a scalable synthesis of ammonia through photochemical reactions, wherein nitrogen-fixing bacterial cells, Azotobacter vinelandii (A. vinelandii), form hybrids with colloidal quantum dots (QDs). Irradiation of the QD-A. vinelandii hybrids with visible light is found to significantly enhance ammonia production efficiency. The inherently low ammonia conversion rate of wild-type A. vinelandii is substantially increased upon incorporation of QDs. This increase is attributed to the electron transfer from QDs within the bacterial cells to intracellular bio-components. We explore the scalability of the QD-A. vinelandii hybrids by conducting the photochemical reaction in a 5 L fermentor under various parameters, such as dissolved oxygen, nutrient supply, and pH. Our findings demonstrate that the QD-A. vinelandii hybrid system in a bioreactor setup achieves an ammonia turnover frequency of 11.96 s^− 1, marking a more than sixfold increase in efficiency over that of nitrogenase enzymes alone. This advancement highlights the potential of integrating biological and nanotechnological elements for scalable ammonia production processes.

Quantum Dot

Ammonia

Bacteria

Azotobacter vinelandii

Fermentation

Ammonia is one of the most produced chemicals in the world, with its demand expanding significantly as both sources for fertilizers and hydrogen-storage media [1–4]. The increasing demand in these areas calls for sustainable synthesis of ammonia. The Haber-Bosch process, a conventional ammonia production process, is energy- and carbon-intensive in such a way that the process itself accounts for approximately 2% of global energy use and emits 2.9 tons of CO₂ for each ton of ammonia produced [5, 6]. Given these substantial energy demands and environmental ramification, there is a pressing need to explore new systems that offer improved energy efficiency and reduced environmental impact for ammonia synthesis.

The quest for sustainable ammonia production has led researchers to explore bio-based methods capitalizing on renewable resources. Azotobacter vinelandii, free-living nitrogen-fixing bacteria, converts atmospheric nitrogen into ammonia under ambient conditions. The nitrogenase synthesizes ammonia through its enzymatic activity at temperatures below 40 ℃ and atmospheric pressure [7–12]. This biological process distinguishes itself from energy-intensive conventional methods by requiring significantly milder reaction conditions. However, the nitrogen fixation reaction orchestrated by these bacteria is inherently complex, resulting in a low ammonia production rate. The conversion of nitrogen to ammonia requires eight electrons and sixteen adenosine triphosphate (ATP) molecules to synthesize two molecules of ammonia [10–14]. The hydrolysis of ATP is the rate-limiting step in the nitrogen fixation reaction [15, 16]. It is of paramount interest to facilitate the electron transfer in this step in order to increase the overall reaction rate of ammonia production from diazotrophs.

Colloidal quantum dots (QDs) are semiconductor nanocrystals in the quantum confinement regime. A set of unique optical and photophysical characteristics, such as size-tunable bandgap of semiconductors, has been the impetus for the precise control of their conduction and valence band energy levels. This property facilitates applications in high-resolution displays and LED lighting with enhanced brightness [17–19]. Additionally, these properties open opportunities in catalysis and environmental applications, where their photoexcited electron-hole pair formation can catalyze chemical reactions [20–27]. In attempts to enhance ammonia synthesis, previous research demonstrated a hybrid system combining cadmium sulfide (CdS) nanorods with nitrogenase enzymes [28, 29]. This system achieved a notable turnover number of 1.1×10⁴ mol NH₃ per mole of MoFe protein under constant light exposure for up to 5 hours to catalyze chemical reactions effectively [28, 29]. However, previous approaches faced limitations due to the need for enzyme purification, the requirement for anaerobic conditions to maintain enzyme activity. Additionally, the use of cadmium-based nanomaterials poses environmental and health risks. Addressing these challenges, our recent study has introduced a novel hybrid structure combining QDs with A. vinelandii [30]. This approach leverages a whole cell system to bypass preprocessing steps such as enzyme purification. The QD-A. vinelandii hybrid system, based on whole cells, not only overcomes the limitations associated with anaerobic activity but also utilizes the metabolic processes of living bacteria for real-time ammonia production under aerobic conditions. Furthermore, we utilized indium phosphide (InP) based QDs, chosen for their biological compatibility due to being cadmium- and lead-free. We have developed a QD-A. vinelandii hybrid by integrating QDs into the bacterial growth process to facilitate their internalization. This system is capable of efficient photoinduced ammonia production, marking a significant step forward in sustainable ammonia synthesis technology.

Producing materials from renewable biomass in biorefineries has become increasingly important for global sustainability goals. This study advances this effort by demonstrating the scalable cultivation of A. vinelandii in fermentors [21, 31, 32]. We facilitated bench scale cultivation of nitrogen-fixing bacteria using a fermentor to examine the system's scalability. Fermentation plays a crucial role in sustainable chemical production, offering solutions to global environmental challenges [7, 33, 34]. The implementation of QD-A. vinelandii hybrid structures in the fermentation process holds great significance.

The effective cultivation of seed bacteria to high concentration of cells is essential. To address these challenges, dissolved oxygen levels and nutrient concentrations in the culture medium were regulated for successful high-density cultivation. Upon reaching maximum bacterial density, light irradiation was applied to activate the QD-A. vinelandii hybrids for ammonia synthesis. This research aims to develop a method for producing ammonia that is both efficient and environmentally sustainable, providing a milder alternative to the existing Haber-Bosch process by using the hybrid of nitrogen-fixing bacteria and QDs.

Materials. Indium acetate (In(OAc)₃, 99.99%), Zinc acetate (Zn(OAc)₂, 99.99%), oleic acid (OA, 90%), 1-octadecene (ODE, 98%), tri-n-octylphosphine (TOP, 97%), tris(trimethylsilyl)phosphine (P(SiMe₃)₃, ≥95%), tetramethylammonium hydroxide pentahydrate (TMAH · 5H₂O, ≥97%), 3-mercaptopropionic acid (MPA, ≥99%), Iron(III) chloride (FeCl₃, anhydrous powder, ≥99.99%), sodium molybdate dihydrate (Na₂MoO₄ · 2H₂O, ≥99.5%), sodium citrate monobasic (anhydrous, ≥99.5%), salicylic acid (≥99%), sodium hypochlorite solution (NaClO, 10-15% chlorine), sodium nitroferricyanide(III) dihydrate (Na₂[Fe(CN)₅NO] · 2H₂O, ≥98%) and Dulbecco′s Phosphate Buffered Saline (D8537, PBS) were purchased from Sigma-Aldrich. Saccharose (sucrose, EP, GR) and sodium hydroxide (NaOH, 97%) were purchased from JUNSEI. Burk’s medium (sucrose (20 g/L), MgSO₄ (0.2 g/L), K₂HPO₄ (0.8 g/L), KH₂PO₄ (0.2 g/L), CaSO₄ (0.13 g/L), FeCl₃ (1.45 mg/L), and Na₂MoO₄ (0.253 mg/L)) was purchased from HIMEDIA. All the purchased chemicals were used without further purification. A. vinelandii (KCTC 2426, ATCC 12837) was obtained from the Korean Collection for Type Cultures.

Colloidal InP/ZnSe Core-Shell Quantum Dots. InP QDs were synthesized via the heat-up method following established procedures [30,35,36]. In a 100 mL three-neck round-bottom flask, 0.45 mmol of In(OAc)₃, 1.35 mmol of OA, and 27 mL of ODE were combined. After degassing at 120 ℃, 2.2 mL of TOP was introduced under argon atmosphere. Following 30 minutes of degassing, the mixture was cooled to room temperature in an argon atmosphere. A solution of 0.3 mmol of P(SiMe3)₃ in 0.9 mL of TOP was injected into the reactor at room temperature, and the temperature was raised to 300 ℃. The InP core was annealed for 5 minutes at 300 ℃ and then cooled to room temperature. For the ZnSe shell, the successive ionic layer adsorption and reaction (SILAR) method was employed. A zinc precursor, consisting of 10 mmol of Zn(OAc)₂, 20 mmol of OA, and 13.7 mL of ODE, was degassed at 120 ℃. After the addition of 5 mL of TOP, further degassing occurred for 30 minutes. The flask was heated to 250 ℃ to form Zinc oleate (Zn(OA)₂) for 30 minutes and cooled to 120 ℃. This process was repeated for cooling to 60 ℃. The Zn(OA)₂ was then injected into the InP core QDs, while 2 M of TOP-Se was wisely dropped as the anion precursors, with the amount calculated based on the relation between the volume of the ZnSe monolayer and the number of core dots. The synthesized QDs were initially dispersed in toluene and underwent purification with ethanol, isopropanol, and butanol as anti-solvents. The QDs were subjected to centrifugation and then redispersed in toluene, repeating this purification process three times. Subsequently, the purified QDs in toluene were mixed with an MPA solution (0.2 M MPA, 0.35 M TMAH · 5H₂O in methanol) and sonicated for 30 minutes. In the ligand exchange process, hexane and acetone served as anti-solvents, and the precipitation process was repeated three times. Finally, the MPA-capped InP/ZnSe QDs were dissolved in deionized water. The synthesized QDs were imaged using field emission transmission electron microscopy (Tecnai F20, FEI Company). Absorption spectra of QDs were recorded using a UV-Vis spectrometer (UV3600, Shimadzu). Emission spectra were obtained with a photoluminescence spectrometer (C11347, Hamamatsu).

Quantum Dot-A. vinelandii Hybrid. A. vinelandii was cultured in a modified Burk’s medium containing adjusted concentrations of FeCl₃ and Na₂MoO₄ to 8 and 2.45 mg/L, respectively [23]. The seed bacteria were transferred to a fresh Burk’s medium with a 1/100 dilution after 30 hours of cultivation at 30 ℃ with agitation at 200 rpm. The QD-A. vinelandii hybrid cells were prepared by co-cultivating bacteria and QDs simultaneously in a culture medium. For making the QD-A. vinelandii hybrid cells, the pre-cultured bacteria were inoculated into the modified Burk’s medium including sterile-filtered QDs and cultured at 30 ℃ with agitation at 200 rpm. The concentration of QDs in the culture medium is set to 50 nM (Fig. S1). The grown cells were washed with cold PBS three times. The optical density at 600 nm (OD₆₀₀) for confirming cell density was adjusted to 2.0 using a TECAN Infinite 200PRO, and then 2 mL of the cell suspension was exposed to light (Supplementary Note 1). The white light sources utilized in the flask scale experiments are OSRAM DULUX L 36W/864 lamps (6500K, 53 mW), and LED panels are used in fermentation experiments, with the spectrum data shown in Fig. S2.

Quantification of Ammonia. To quantify ammonia concentrations in cell culture supernatants, the indophenol blue colorimetric method was employed [30,37]. Cell culture supernatants were obtained by diluting cell cultures in PBS, and supernatant was collected for analysis. Standard ammonium ion solutions with known concentrations were prepared for the calibration curve and the calibration curve was drawn for each quantification to enhance the reliability. Indophenol blue reagents were added sequentially to each standard solution and supernatant of samples. The reaction was allowed to proceed for 2 hours at room temperature and the absorbance measurements were conducted at 655 nm using a spectrophotometer.

Fermentation. In this study, A. vinelandii was cultivated at the fermentor, which is a bioreactor. Unlike microbial cultivation at the flask scale, certain factors are essential to optimize bacterial growth in fermentor. The prepared A. vinelandii in 200 mL of modified Burk’s medium as seed bacteria was inoculated into the modified Burk’s medium and sterile-filtered QDs. The pH was maintained at 7.50 using 1 M NaOH. To ensure optimal conditions, the fermentation process was carried out at a temperature of 30 ℃. The dissolved oxygen (DO) level was controlled through the regulation of air flow rate and agitation. Throughout the fermentation, cell density was monitored using UV-Vis spectroscopy, measuring the optical density at a wavelength of 600 nm. The bacterial fermentation was performed using Liflux GX equipment by Hanil Science. The concentration of sucrose was measured by HPLC (1515 isocratic HPLC pump, Waters) equipped with a refractive index detector (2414, Waters) and MetaCarb 87H column (Agilent).

Colloidal Quantum Dots as Photosensitizers. We introduce a system for producing ammonia by integrating QDs within bacteria and applying light irradiation to the QD-A. vinelandii hybrids, as shown in Fig. 1a. Harnessing QDs as photosensitizers in photochemical reactions requires the design and synthesis of QDs with facile charge extraction capabilities. In this research, core-shell structured QDs were engineered with water-dispersible ligands for efficient interaction in a whole cell system. InP core QDs were uniformly synthesized using the heat-up method. The synthesis of ZnSe shells via the successive ionic layer adsorption and reaction (SILAR) method resulted in a quasi-type II bandgap structure in the core-shell QDs [30,35,36,38]. Furthermore, the oleic acid ligands on the surface of the QDs were replaced with mercaptopropionic acid to improve their dispersion and reactivity of QDs in aqueous solutions. The absorption and photoluminescence spectra of the InP/ZnSe core-shell QDs, as depicted in Fig. 1b, explain the optical properties of QDs. Notably, the 1S peak wavelength of the InP core, detailed in Fig. S3, is observed at 460 nm, indicating a bandgap energy of approximately 2.70 eV for the core QDs. An increase in shell thickness leads to a decrease in the quantum confinement effect and lowers the energy level at the conduction band edge. This increase in shell synthesis leads to the formation of the quasi-type II bandgap alignment, a critical feature designed to improve electron extraction capabilities significantly [39]. The characterization of these QDs reveals their distinct sizes as visually confirmed by the transmission electron microscopy (TEM) image in Fig. 1c.

Influence of Light Sources on Cell Viability. Ammonia production efficiency under a 400 nm light source reached saturation after 6 hours. This outcome indicates limited ammonia productivity under 400 nm light, hypothesized to result from cellular damage. 400 nm light sources, known to generate reactive oxygen species (ROS) within cells, potentially compromise cellular viability [40-42]. To address these challenges and enhance the overall efficiency of the hybrid system, experiments utilized white light, chosen for its high light absorption capabilities of QDs and optimized wavelength to minimize cellular damage.

Ammonia production under white light irradiation continued to increase and this demonstrated an extended productive phase compared to 400 nm light conditions (Fig. 2a). Unlike the results obtained with 400 nm light exposure where ammonia production reached saturation at 6 hours, the QD-A. vinelandii hybrid cells exposed to white light demonstrate a continuous increase in ammonia production for up to 12 hours. In Fig. 2b, the number of viable cells over time during the ammonia production reaction is shown, with data comparing the effects of various light sources on cell density. Notably, a significant decline in cell viability under 400 nm light was observed around the 4-hour mark, in contrast to cells maintained in dark. In comparison, bacteria exposed to white light resulted in a substantially higher survival rate than the case of 400 nm light irradiation. This condition effectively delayed the saturation of ammonia production. Nitroblue tetrazolium (NBT) was employed to compare the amount of generated ROS in QD-A. vinelandii cells. The NBT assay allows comparison of ROS levels by observing changes in absorbance at 560 nm. These changes result from the formation of reduced form of NBT, known as NBT formazan [43,44]. Under all conditions, ROS generation was detectable with or without QDs. Cells exposed to 400 nm light showed higher ROS generation than those under dark or white light conditions (Fig. 2c). This result supports the previous assumption that the elevated levels of cellular ROS production under 400 nm light could inflict damage on the cells.

Furthermore, an investigation was conducted on the ammonia synthesis by bacteria under illumination in the absence of QDs, to ascertain that the observed enhancement in production stemmed from photoexcited charges elicited by the QDs, rather than from mere light exposure (Fig. S4). The experiments resulted in no increase in ammonia production when only light was applied, indicating that the enhancement in ammonia production is directly or indirectly attributed to the photoexcited charges generated by the QDs.

Effect of Growth Medium and Nutrients on Ammonia Production. In ongoing experimental investigations, the ammonia synthesis system of dispersed hybrid cells in phosphate buffered saline (PBS) was conducted after removing the nutrient media. Ammonia production was not observed under conditions of nutrient-rich media. This observation leads to the hypothesis that bacteria, when provided with ample nutrients, preferentially engage in metabolic activities related to biomass formation. The research focused on assessing the roles of sucrose and magnesium (Mg) in the ammonia production efficiency of QD-A. vinelandii hybrids. Sucrose serves as the primary carbon source for cellular growth and energy production. Mg is essential for enzyme activation, maintaining cellular and genetic integrity, and efficient nitrogen fixation [45].

Adding carbon resources to the PBS buffer did not enhance ammonia production. This suggests that providing carbon is insufficient to stimulate ammonia synthesis in the hybrid cells (Fig. 3a). Conversely, Fig. 3b shows that removing sucrose from Burk's medium resulted in increased ammonia productivity. This indicates that sucrose supply can influence metabolic shifts within the cells. Under conditions rich in nutrients, bacteria appear to prioritize biomass formation (Fig. S5). This process leads to the continuous utilization and subsequent depletion of any ammonia produced, making it nearly undetectable. In contrast, under PBS conditions with limited essential carbon sources, bacteria shift their metabolic focus, preventing biomass formation and enabling ammonium ion accumulation. The absence of sucrose might mitigate a competitive metabolic pathway, thereby enhancing the efficiency of ammonia synthesis. These observations highlight the importance of a delicate balance between nutrient availability and metabolic activity for the optimization of the QD-A. vinelandii hybrid system for ammonia production. Further experimentation involved subjecting a series of hybrid cell cultures to a single feeding of sucrose at different reaction times for up to 12 hours. The results shown in Fig. S6 revealed that cells supplemented with sucrose early in the reaction period produced the least ammonia. Conversely, samples fed sucrose at later stages, particularly at 9 hours, demonstrated increased ammonia production, closely rivaling that of cultures without any sucrose feeding. This emphasizes the importance of balanced nutrient management in optimizing the QD-A. vinelandii hybrid system for efficient ammonia synthesis.

Further analysis on the effect of Mg supplementation or its removal showed that ammonia productivity remained consistent. This suggests that Mg does not significantly influence ammonia production in the QD-A. vinelandii hybrid system. As shown in Fig. 3c, this observation highlights the pivotal contribution of QDs, possibly via photoinduced charge transfers, in the ammonia synthesis process, surpassing traditional nutrient factors such as Mg. The minimal impact of Mg on ammonia production indirectly validates the critical contribution of QDs to the system. Their important roles in enhancing ammonia synthesis efficiency are paramount.

One-Pot Synthesis of Ammonia Using QD-A. vinelandii Hybrid. Despite sucrose's ability to promote bacterial proliferation, our insights reveal that removing sucrose establishes optimal conditions for enhanced ammonia synthesis. Building on these insights, we proposed a separated process comprising a cultivation step conducted in dark conditions—allowing QD-A. vinelandii to sufficiently internalize and grow while depleting sucrose in the culture medium—and a subsequent production step induced by light exposure to generate ammonia. The overview of this two-step process is depicted in Fig. 4a.

Furthermore, appropriate dissolved oxygen levels were crucial for the fermentation of A. vinelandii, an aerobic bacterium with enzymes that are active under anaerobic conditions. The anaerobic bacteria require a balanced air supply for optimal growth and ammonia production. In experiments comparing bacterial growth across DO levels from 10-40%, we observed that a controlled DO level at 10% (Fig. 4b) facilitated the conditions needed for both biomass formation and efficient ammonia synthesis. This adjustment in oxygen levels reflects a strategic approach to optimizing the conditions for ammonia production without compromising bacterial growth.

In the conducted fermentation experiments, an elevated level of ammonia production was observed through the QD-A. vinelandii hybrid system, as shown in Fig. 4c. A. vinelandii cultured in a nutrient medium containing QDs and sucrose under dark conditions, exhibited growth with an OD₆₀₀ value of approximately 23, which corresponds to 3.71 g/L of dry cell weight (DCW). Subsequently, the sucrose in the culture medium was completely depleted and light irradiation was started to stimulate ammonia production. The amount of ammonia produced reached approximately 7.8 mg/L for a 45-hour reaction period, significantly surpassing the turnover frequency (TOF) of enzymes responsible for ammonia generation within conventional nitrogenase in nitrogen-fixing bacteria. The TOF, calculated by dividing the moles of synthesized ammonia per time by the moles of MoFe protein, showed our hybrid system's TOF value to be an impressive 11.96 s^-1, with the moles of MoFe protein per DCW approximated to 9.02 × 10^-11 (Fig. 4d and Supplementary Note 2). This demonstrates a remarkable difference in ammonia productivity by over sixfold compared to conditions using purified MoFe proteins with the presence of Fe proteins and ATPs [21]. Specifically, the fermentation of the QD-A. vinelandii hybrid system resulted in ammonia production with a titer of 7.81 mg/L, a yield of 7.41 mmol/mol, and a productivity of 0.174 mg/L/h. Our approach has led to significant advancements and efficiency in ammonia synthesis. It highlights the potential of the QD-A. vinelandii hybrid system for enhancing bioengineering applications.

This study presents a scalable approach to ammonia production using hybrid of QDs and nitrogen-fixing bacteria in fermentors. Our comprehensive investigation of the QD-A. vinelandii hybrid system yielded valuable insights into optimizing the fermentation conditions of A. vinelandii. The research progressed from laboratory scale experiments to bench scale studies, representing a significant advancement toward the practical implementation of this system.

The uptake of core-shell structured QDs into A. vinelandii enhances charge dissociation probability, which is pivotal for efficient photochemical reactions. The transition to white light as a source minimized phototoxic effects on the bacteria, and effectively prolonged ammonia production beyond the constraints of conventional 400 nm irradiation. Additionally, the presence of sucrose led to ammonia consumption for biomass formation, with no increase in ammonia productivity upon its depletion. Importantly, our comparison of ammonia production efficiency with Mg content indirectly confirmed the role of QDs in enhancing ammonia synthesis. Building on these results, we applied these findings to scale up and optimize fermentation processes, adjusting various factors as necessary. These modifications, combined with maintaining a 10% DO level and utilizing a sucrose-free Burk’s medium, significantly enhanced bacterial growth and ammonia synthesis efficiency. Furthermore, we developed a two-step fermentation process involving a dark cultivation phase followed by a light-exposed production phase, effectively mitigated bacterial growth inhibition under continuous light exposure.

These findings significantly advance QD-A. vinelandii hybrid applications in sustainable ammonia synthesis. The integration of nanomaterials and biological systems holds great promise for environmentally benign technologies.

Acknowledgements

This work has been supported by the Samsung Research Funding & Incubation Center of Samsung Electronics under Project Number SRFC-MA2001-07, the National Research Foundation of Korea (NRF) under Project Number 2022R1A5A1033719 and 2022M3J5A1056117, and the Korea Planning & Evaluation Institute of Industrial Technology (KEIT) under Project Number 20019417.

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