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Biological Self-Assembled Transmembrane Electron Conduits for High-Efficiency Ammonia Production in Microbial Electrosynthesis
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Bioremediation and Biotechnology

Biological Self-Assembled Transmembrane Electron Conduits for High-Efficiency Ammonia Production in Microbial Electrosynthesis
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  • Yao Li
    Yao Li
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    More by Yao Li
  • Sen Qiao*
    Sen Qiao
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    *Email: qscyj@mail.dlut.edu.cn
    More by Sen Qiao
  • Meiwei Guo
    Meiwei Guo
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    More by Meiwei Guo
  • Liying Zhang
    Liying Zhang
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    More by Liying Zhang
  • Guangfei Liu
    Guangfei Liu
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    More by Guangfei Liu
  • Jiti Zhou
    Jiti Zhou
    Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    More by Jiti Zhou
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Environmental Science & Technology

Cite this: Environ. Sci. Technol. 2024, 58, 17, 7457–7468
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https://doi.org/10.1021/acs.est.3c10897
Published April 20, 2024
Copyright © 2024 American Chemical Society

Abstract

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Usually, CymA is irreplaceable as the electron transport hub in Shewanella oneidensis MR-1 bidirectional electron transfer. In this work, biologically self-assembled FeS nanoparticles construct an artificial electron transfer route and implement electron transfer from extracellular into periplasmic space without CymA involvement, which present similar properties to type IV pili. Bacteria are wired up into a network, and more electron transfer conduits are activated by self-assembled transmembrane FeS nanoparticles (electron conduits), thereby substantially enhancing the ammonia production. In this study, we achieved an average NH4+-N production rate of 391.8 μg·h–1·L reactor–1 with the selectivity of 98.0% and cathode efficiency of 65.4%. Additionally, the amide group in the protein-like substances located in the outer membrane was first found to be able to transfer electrons from extracellular into intracellular with c-type cytochromes. Our work provides a new viewpoint that contributes to a better understanding of the interconnections between semiconductor materials and bacteria and inspires the exploration of new electron transfer chain components.

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Copyright © 2024 American Chemical Society

Synopsis

This study broke the conventional view that CymA protein was irreplaceable in extracellular electron transfer in Shewanella oneidensis MR-1.

Introduction

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Ammonia (NH3) is an essential raw material for industry and agriculture. (1) According to the International Energy Agency (IEA), ammonia production is around 200 million tons per year and 85% of them is consumed as a feedstock for nitrogen fertilizer. (2) Lately, NH3 is also considered as an alternative fuel and energy storage carrier due to superior gravimetric hydrogen density (17.8 wt %) and sizable volumetric energy density (15.6 MJ L–1). (3) The traditional ammonia industry (Haber–Bosch process) requires an internal temperature over 800 °F and a pressure of about 200 atm, which demands enormous energy (approximately 1.8% of the world’s energy consumption) and resulted in 235 million tons of CO2 emissions annually (about 1.4% of global CO2 emissions). (4,5)
Electrosynthesis of ammonia is an alternative way forward for NH3 production via reducing nitrate (NO3), which has a more substantial solubility (92 g/100 g water) and a lower N═O rupture energy (204 kJ mol–1) compared to N2. (6,7) Furthermore, NO3 pollution harms human health and environmental sustainability by producing carcinogenic nitrosamines, causing methemoglobinemia and eutrophication. (8) Electricity-driven NO3-to-NH3 conversion is an attractive approach in terms of saving fossil fuels, yet still limited by low product selectivity in neutral and acidic environment. (9)
The emerging microbial electrosynthesis (MES) systems, which integrate the merits of electronic materials with biocatalysts (electrotrophs), offer innovative opportunities by overcoming the limitations of chemical catalysts. Biocatalysts have the exclusive advantage of high selectivity and mild reaction conditions, as well as being reproducible. (10) Recently, our group injected electrons from cathodes directly into Shewanella oneidensis MR-1 wild-type strain (S. oneidensis) by reversing the typical extracellular electron transfer (EET) chain, developing the cathode-dependent dissimilatory nitrate to ammonia (DNRA) process. (11) Unlike conventional chemical catalysts in which multiple intermediates (such as NO2, NO, and NH2OH) are present in the multielectron transfer process, the DNRA process stepwise reduces nitrate to nitrite and nitrite to ammonium. (12) However, the EET chain is unwired due to the inherited 3D cell structure, thus limiting the performance. (13) Given that the Fe–S cluster tends to act as a cofactor for electron transfer proteins, it is a scientific gap whether electrons could be transferred to terminal enzymes in the periplasmic space via biosynthesized FeS without CymA involvement (indispensable inner membrane protein in outward EET). (14) If as our expectation, electron transfer rate and cathode efficiency could be expedited, we could further implement highly efficient MES.
Herein, we report a strategy of biosynthesized FeS nanoparticles (NPs) as wired electron transfer conduits at the interface between the cell and the cathode, designing S. oneidensis@FeS hybrid systems to address the limitation of transmembrane electron transport for improving the NH3 production performance. The well-designed hybrid system demonstrated the dramatically enhanced electron uptake efficiency and allowed inward EET no longer relying on CymA solely. As a proof of concept, the biohybrid system achieved an average NH4+-N production rate of 391.8 μg·h–1·L reactor–1 with the average selectivity of 98.0% and an average cathode efficiency of 65.4%. The study offers an interesting perspective into the interconnections between semiconductor materials and bacteria, inspires the exploration of new electron transfer chain components, and opens an avenue for achieving environmentally friendly and high-efficiency conversion of NO3 to NH3 with ultrahigh product selectivity.

Materials and Methods

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Biosynthesis of FeS Nanoparticles

An overnight suspension of S. oneidensis was inoculated into Luria–Bertani broth at a ratio of 1:100 and incubated at 30 ± 1.0 °C for approximately 12 h to reach the end of the logarithmic growth phase. Residues were rinsed using a 0.01 M phosphate buffer solution (PBS). FeS biosynthesis experiments were performed in 100 mL bottles containing M9 salt medium supplemented with 0.50 g/L yeast extract, 0.25 g/L peptone, 18 mM sodium lactate, 2 mM Fe(III)-citrate, and different concentrations of Na2S2O3 (0, 0.5, 1, 2, 4, and 8 mM) for 24 h. To maintain anaerobic conditions, each bottle was purged with nitrogen for 20 min and subsequently sealed with butyl rubber stoppers and aluminum caps. S. oneidensis was introduced into the bottle with an initial optical density (OD600) of 0.5. The bottles were incubated at 30 ± 1.0 °C on a shaker table (180 rpm). During the incubation, samples were collected periodically to monitor the Fe(II) concentration. Before the experiment, all glassware was sterilized in an autoclave (LDZX-30KBS, Shenan, China) at 121 °C for 20 min. The sample collection and pretreatment steps were carried out within an anaerobic glovebox (YQX-II, CIMO, China). Depending on the electrochemical analysis results, we chose the most suitable biosynthesis conditions for subsequent experiments. Details are shown in Figures S1–S3.

Preparation of Artificial Biofilms

Following biosynthesis, the bacteria were centrifuged with 0.1 M PBS at 10,000 rpm for 5 min and washed thrice. Then, they were subsequently adjusted to the same level (0.5 mg of protein) with 4 mL of PBS. A 200 μL Nafion membrane solution as an immobilization agent was added to the bacterial solution to encapsulate S. oneidensis. Artificial biofilms were created by uniformly dropping all the bacterial solution onto carbon felts (60 × 60 × 2 mm) and then air-dried under 30 ± 1.0 °C for 6 h. (15) The entire procedure was carried out under aseptic and anaerobic conditions.

Microbial Electrosynthesis System Setup and Operation

Artificial biofilms were employed as cathodes in a MES system with a potentiostat (DJS-292, Leici, China), applying a constant voltage of −0.41 V vs SHE. After gently sparging with helium gas for 20 min to remove dissolved oxygen, three parallel MES reactors were sealed and operated at 30 ± 1.0 °C in a shaker table (150 rpm). Figure S4 illustrates the use of carbon felts as electrode materials. The counter electrode (anode) was measured as 60 × 80 × 2 mm, while the working electrode (biocathode) had dimensions of 60 × 60 × 2 mm. To pretreat the carbon felt, a sequential treatment was conducted using 1 M sulfuric acid, ultrapure water, and 1 M acetone to remove surface-deposited inorganic particles, metal ions, and organic residues. This was followed by heating at 450 °C for 30 min in a muffle furnace (TM-0914, Meicheng, China) to enhance thermal stability and eliminate impurities. (16) The practical operational volume of the dual-chamber reactor was 200 mL, and the distance between the cathode and the anode was 12 cm. The two chambers were divided by a proton exchange membrane (Nafion 117, Dupont, USA), which was consecutively pretreated with 5% hydrogen peroxide, ultrapure water, and 5% sulfuric acid at 80 °C for 1 h. (17) Prior to the experiments, all glassware and metal components were subjected to sterilization. The Ag/AgCl electrode (+197 mV vs SHE) was immersed in 70% alcohol for 6 h and sterilized on a clean bench under UV irradiation (ZHJH-1115B, Zhicheng, China). The composition of the electrolyte solution is shown in Table S1. In each cycle, S. oneidensis and S. oneidensis@FeS systems were operated for 5 and 3 days to allow as much nitrate reduction as possible. At the end of each cycle, a sterilized 0.1 M PBS solution was employed to wash the anode and cathode chambers thrice. Afterward, the sterile electrolyte solution was readded for the next cycle. The complete MES experiment was run for three cycles, respectively.

Characteristics of the Biosynthesis-FeS and Biohybrid

The morphologies of the S. oneidensis and S. oneidensis@FeS systems were examined by a scanning electron microscope (SEM, SU5000, Hitachi, Japan). The samples were centrifuged with 0.1 M PBS at 10,000 rpm for 5 min and washed three times and then fixed with 2.5% (v/v) glutaraldehyde solution at 4 °C for 12 h. After that, they were gradient dehydrated by centrifugation at 10,000 rpm for 5 min in various ethanol concentrations (0, 20, 40, 60, 80, 90, 95, 100% (v/v)) and dispersed in ultrapure water, and then 20 μL was taken on a silicon wafer (3 × 3 mm), leaving the samples to dry and spraying platinum for SEM observation. Elemental analysis was conducted utilizing energy-dispersive X-ray spectroscopy. The size distribution of biosynthesis-FeS was analyzed by image analysis software (Nano Measurer), with a minimum of 100 NPs measured in each image for statistical analysis. Ultrathin cell slices were mounted on copper grids for high-angle annular dark-field scanning transmission electron microscopy (HAADF-STEM) image capture and elemental analysis (HT7700, Hitachi, Japan) at an acceleration voltage of 200 kV. Before observation, samples were washed by centrifugation, fixed and gradient dehydrated (as described previously), and then stained with osmic acid and impregnated with epoxy resin. Subsequently, the samples were sliced by ultramicrotome. The biohybrids at different precursor concentrations were characterized by ultraviolet–visible near-infrared spectroscopy (UV–vis-NIR, SolidSpec-3700, Shimadzu, Japan). For crystal structure, the vacuum freeze-dried powder of samples was subjected to X-ray powder diffraction spectroscopy (XRD, D8 Advance, Bruker, Germany). The valence states were determined through X-ray photoelectron spectroscopy (XPS, ESCALAB XI+, Thermo, UK).

Electrochemical Measurement and Analysis

A data acquisition card (DAQM-4212, Zhouzheng, China) measured the current in the dual-chamber reactors. The current density (J, A/m2), total accumulated electrons (C, A·S), cathode efficiency (ηE, %), and selectivity (%) were calculated according to the following equations:
J=IS
(1)
C=0TIdt
(2)
ηE=F×V×(n1×ΔNH4+N+n2×ΔNO2N)/(1000×M)0TIdt×100%
(3)
selectivity=ΔNH4+NΔNO3N×100%
(4)
where I (A) shows the cathode current; S (m2) indicates the cathode area; T (s) is the reaction time per cycle; F denotes the Faradaic constant (96485.3 C/mols); V (L) represents the reaction volume; n1 and n2 (mols/mol) express the numbers of electrons per mole of nitrate reduced to ammonia and nitrite, respectively; ΔNH4+-N, ΔNO2-N, and ΔNO3-N (mg/L) are the concentration variations of N in ammonia, nitrite, and nitrate, separately; and M (g/mol) refers to the relative atomic mass of nitrogen.
The electrochemical property of the biocathode was analyzed by cyclic voltammetry (CV) and electrochemical impedance spectroscopy (EIS) with an electrochemical workstation (CHI660E, Chenhua, China). CV was performed in 0.1 M PBS from −0.8 to 0.6 V vs Ag/AgCl at a scan rate of 50 mv/s, and EIS was carried out over a frequency range of 100 kHz to 0.01 Hz with a sinusoidal perturbation amplitude of 5 mV. Equivalent circuit and resistance values were defined by ZView software. For biohybrids with different precursor concentrations, 10 mL of the bacteria solution after 24 h biosynthesis was taken as well as centrifuged and washed three times with 0.1 M PBS at 10,000 rpm for 5 min. Afterward, they were dispersed in 1 mL of PBS containing 50 μL of Nafion solution. Finally, 100 μL was taken from it and coated on the surface of pretreated carbon felt (10 × 10 × 2 mm) as the working electrode. The cathodic biofilm, platinum sheet electrode (1.5 × 1.5 cm), and Ag/AgCl electrode were the working, counter, and reference electrodes, respectively. Before electrochemical measurement, the electrolyte was aerated with N2 for 20 min to remove dissolved oxygen and the unit was set to open circuit for 2 h.

Biofilm Spatial Morphology Test

The state of the cathode biofilm was visualized with confocal laser scanning microscopy (CLSM, FV1200, Olympus, Japan). In order to dye the biofilm, a LIVE/DEAD BacLight Bacterial Viability Kit was applied. The biofilm samples were gently rinsed twice with sterile saline, and 0.5 mL of staining solution (2 mL of sterile saline with 2 μL of SYTO-9 and 4 μL of PI) were added dropwise to the sample surface and incubated for 15 min at 37 °C protected from light. The staining solution was washed with sterile saline after staining. Details are shown in Figures S5 and S6.

Molecular-Level Tests for Surface Group

Artificial biofilms were employed as the working electrode for the electrochemical in-situ Fourier transform infrared spectroscopy test. An electrochemical workstation (CHI660E, Chenhua, China) provided the working potential with a gradient ranging from −0.9 to 0.4 V vs Ag/AgCl. A Fourier transform infrared spectroscopy spectrometer (VERTEX 70, Bruker, Germany) was applied. Additionally, a Ag/AgCl electrode and a Pt sheet were used as the reference and counter electrodes, respectively. All electrodes were placed into the IR cell to form a single-chamber reactor, and 0.1 M D2O was utilized as the electrolyte to mitigate any spectral dose effects.

Other Analysis

The concentrations of NO3-N, NO2-N, and NH4+-N were determined by a spectrophotometer (SPECORD 50 PLUS, Analytik Jena AG, Germany) with the salicylic acid method, ethylenediamine dihydrochloride colorimetric method, and sodium hypochlorite–salicylic acid method, respectively. (18,19) The Fe(II) concentration was measured via o-phenanthroline spectrophotometry. (20) The total nitrogen concentration in the electrolyte was calculated as the sum of the nitrate, nitrite, and ammonia. In order to measure the total organic carbon (TOC), a TOC and total nitrogen analyzer (multi N/C 2100S, Analytik Jena AG, Germany) was employed. The Bradford Protein Assay Kit (C503031, Sangon Biotech (Shanghai) Co., Ltd.) was utilized to quantify the protein content.

Results and Discussion

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Characteristics of the Biosynthesis-FeS

The microstructure, crystalline phase composition, and elemental valence states of the S. oneidensis@FeS system were analyzed by SEM, HAADF-STEM, XRD, and XPS, respectively. In the biohybrid system, the spherical NPs were uniformly anchored on the bacterial surface and wrapped tightly around the bacterial cell compared to the control group (Figure 1A,B). Elemental mapping revealed sulfur and iron as the main elements in the NPs (Figure S7), with a mean particle size of 37.1 ± 8.2 nm (Figure 1C). In this dimensional range, the biohybrid systems were reported to have the most extraordinary electron transfer efficiency. (21) According to the HAADF-STEM images after the cell slice, FeS NPs emerged as bright white dots, and they accessed into the intracellular environment (Figure 1D–G). This spatial morphology allowed FeS NPs to bridge the intracellular and extracellular environments, probably dramatically facilitating the electron transfer. (001), (101), and (200) facets as typical peaks indicated that the NPs were mackinawite FeS (Figure 1H). Therein, poor crystallinity was associated with insufficient low ambient pH and solid growth duration. (22) Three types of chemical bonds occurred in the fitted curves with the Fe2p3/2 spectra: Fe(II)–S (707.2 eV), Fe(II)–O (709.7 eV), and Fe(III)–S (711.3 eV) (Figure 1I). Moreover, in the S2p spectra, the peaks are attributed to S2– (160.9 eV) and S22– (162.1 eV) (Figure 1J). The absence of other sulfur-containing substances (e.g., SO32–, S0, and Sn2–) indicated a high-selectivity biosynthesis of FeS NPs. (23)

Figure 1

Figure 1. Characteristics of the S. oneidensis@FeS system.

SEM images of (A) S. oneidensis and (B) S. oneidensis@FeS (scale bars: 100 nm). (C) The FeS NP size distribution. (D) HAADF-STEM image of the sliced S. oneidensis@FeS (scale bars: 200 nm) and (E–G) EDS mapping of the sliced S. oneidensis@FeS (scale bars: 200 nm). (H) XRD spectra of S. oneidensis@FeS. (I, J) XPS spectra of the S. oneidensis@FeS.

Ammonium Production Performance

The MES systems were operated under a constant potential of −0.41 V vs SHE in order to prevent hydrogen evolution (Figure S4). (24) This low applied voltage aimed to avoid the interference of hydrogen as an electron donor for S. oneidensis and to maximize cathodic electron uptake for nitrate reduction. (25) NO3 removal performance is shown in Figure 2A,B by S. oneidensis and S. oneidensis@FeS systems with the identical initial NO3-N concentration of approximately 20.0 mg/L. During the reaction, TOC concentrations in both systems were stabilized around 1.0 mg/L without obvious fluctuations, excluding the contribution of organic carbons (Figure S8). Moreover, the nitrate reduction occurred stepwise to nitrite and then nitrite to ammonium, with the cathode as the sole electron donor, and the total nitrogen amount was maintained in equilibrium, consistent with previous studies. (11,12,26) Compared to S. oneidensis, S. oneidensis@FeS system completely reduced NO3 to NH4+ within 72 h without NO2 accumulation, whereas the former still exhibited an average of 3.1 mg/L NO2-N left in the 120 h reaction period. In addition, the S. oneidensis@FeS system achieved a superior selectivity (the maximum of 99.1%) and NH4+-N production rate (the maximum of 395.0 μg·h–1·L reactor–1) in three cycles (Figure 2C,D). For S. oneidensis, the selectivity and NH4+-N production rates reached maximum values of 93.7% and 212.0 μg·h–1·L reactor–1, respectively; these were significantly lower than those of the S. oneidensis@FeS system.

Figure 2

Figure 2. Nitrate reduction performances in S. oneidensis and S. oneidensis@FeS systems.

NO3-N, NO2-N, and NH4+-N concentrations in the (A) S. oneidensis and (B) S. oneidensis@FeS system. Yield evaluation of the DNRA process in (C) S. oneidensis and (D) S. oneidensis@FeS system. Each experiment was performed in triplicate, and error bars indicate the standard deviation.
In order to further clarify the role of FeS NPs in reversed EET, mutant strains (ΔomcA/mrtC and ΔcymA) were utilized for measurement, since both omcA/mtrC and cymA were critical proteins in EET of S. oneidensis. (27) Figure S9 illustrates FeS NPs (black solids) could be biosynthesized by both S. oneidensis MR-1 mutants. In mutant strains, NPs were embedded in the outer membrane and aligned in the periplasmic space (Figure S10). In contrast to the wild-type strain (referring to S. oneidensis in the above paragraph, no gene knockout), they still performed a superior role in nitrate reduction (Figure 3A–C). Similarly, the DNRA process was stepwise, with no dramatic fluctuations in TOC concentration (Figure S11). The sterilized S. oneidensis@FeS system was deprived of the ability to electrosynthesize ammonia, suggesting that the nitrate reduction was attributed to S. oneidensis rather than FeS NPs. Considering that CymA served as an important electron transfer hub in the reversed EET, ΔcymA exhibited negligible nitrate reduction activity. (11,28) Furthermore, paralogs (e.g., MtrF) somewhat compensated for the absence of OmcA and MtrC, enabling ΔomcA/mrtC to have a complete EET chain, although their selectivity (33.4%) and NH4+-N production rate (123.8 μg·h–1·L reactor–1) were considerably lower than those of the wild type (S. oneidensis without any knockout processing) (Figure 3D). On the other hand, ΔomcA/mrtC-FeS and ΔcymA-FeS mutant strains biohybrid systems exhibited an unexpectedly substantial ammonia synthesis performance (selectivity: 97.1 and 39.2%, NH4+-N production rate: 103.7 and 202.3 μg·h–1·L reactor–1). Generally, CymA protein has been always viewed as the indispensable hub to the EET process in S. oneidensis MR-1, especially in outward electron transfer. (29) However, the ΔcymA-FeS biohydrid system exhibited satisfactory ammonia production performance without CymA protein involvement, which directly demonstrated that the artificial conduits constructed by FeS NPs were able to carry out inward electron transfer from the cathode to the targeted proteins (NapA, NapB, and NrfA) located in periplasmic space.

Figure 3

Figure 3. Nitrate reduction was by different mutants. (A) NO3-N, (B) NO2-N, and (C) NH4+-N concentrations. (D) Yield assessment. Each experiment was performed in triplicate, and error bars indicate the standard deviation.

Cathodic Electron Consumption

The current density was recorded under the constant potential for three cycles and is plotted in Figure 4A,C. The fluctuating current density indicated a reduction reaction occurring on the cathode biofilm. Initially, sufficient electron acceptors resulted in a gradual electron augmentation. Subsequently, the contradiction between the diminishing reduced substance supply to the electrode and the high electron feed progressively weakened the current density. (30) The S. oneidensis@FeS system had a greater average current density (−0.36 A/m2) in three cycles than that in S. oneidensis (−0.27 A/m2). The total cumulative coulomb amount was determined by integrating the current–time curve (Figure 4B,D). The prolonged reaction time allowed S. oneidensis to have more accumulated electrons (416.0 vs 329.8 A·s). However, the inferior bioelectrochemical reduction capacity resulted in an average cathode efficiency of only 46.5%, much less than that of the S. oneidensis@FeS system (65.4%) (Figure 4E). In Figure 4F, a comparison of ammonia production in different MES systems using nitrate as an electron acceptor is presented. This study stands out as it achieved the most remarkable performance in ammonia production, boasting a superior selectivity of 98.0% and a cathode efficiency of 65.4%, surpassing the results of previous studies. (11,31−35) When N2 was the electron acceptor, this work is even more superior. When activated sludge from a wastewater treatment plant was used as the biocatalyst, the selectivity was reported up to 9.62% (this work was 98.0%). (36) Furthermore, in another study, where long-term domesticated electroactive microorganisms were used to form cathodic biofilms, the cathode efficiency was 4.21% and the NH4+-N production rate was 0.252 μg·h–1·cm–2, only 23.3% of this work (1.081 μg·h–1·cm–2). (37) Although pure bacteria (Pseudomonas stutzeri) improved the cathodic efficiency to some extent (15%), there was a considerable gap compared to nitrate as an electron acceptor. (38)

Figure 4

Figure 4. Cathodic electron consumption in MES systems. Current density and coulomb in (A, B) S. oneidensis and (C, D) S. oneidensis@FeS systems. (E) Cathode efficiency and (F) a comparison of achievements.

In general, the trend of current density in the mutant strains was similar to that of the wild type (S. oneidensis without any knockout processing) (Figure 5A). The sterilized biohybrid system and ΔcymA maintained the current density at a low level and did not fluctuate due to the lack of biocatalysts as well as the intact EET chain, respectively. Correspondingly, the accumulated electrons for sterilized and ΔcymA were 0.3 and 1.5 A·s, which was considerably insufficient for nitrate reduction (Figure 5B). Compared to ΔcymA, ΔomcA/mrtC accumulated more electrons (107.1 A·s). The biosynthesized FeS NPs dramatically enhanced the electron uptake by different mutant strains, with ΔomcA/mrtC-FeS and ΔcymA-FeS values of 209.0 and 117.4 A·s. The current study revealed that the presence of paralogous (MtrF) resulted in the deletion of OmcA and MtrC not significantly affecting EET. (39) In the ΔomcA/mrtC-FeS system, FeS NPs not only compensated for their deficient function but also exhibited superiority over the wild-type strain (S. oneidensis without any knockout processing). In addition, this work illustrated that CymA was not indispensable in the inward EET when biologically self-assembled transmembrane electron conduits (FeS NPs) were available. Regarding electron utilization efficiency, the biohybrid systems likewise played a massive positive role (Figure 5C). The cathode efficiency of ΔomcA/mrtC-FeS was 54.9%, which was 17.9% higher than that of ΔomcA/mrtC, while the cathode efficiency of ΔcymA-FeS (44.4%) was also as 24.7-fold high as that of ΔcymA (1.8%).

Figure 5

Figure 5. Cathodic electron consumption by different mutants. (A) Current density, (B) Coulomb. (C) Cathode efficiency.

Electrochemical Analysis

At the beginning and end of experiments, the biocathode was evaluated by CV and EIS to study the evolution of electrochemical properties during three cycles. CV indicates the electron transfer between the cathode and the biofilm. (40) The curves displayed a characteristic sigmoidal shape, implying superior bioelectrocatalysis in the presence of electron acceptors (Figure 6A,E). The midpoint potential, denoted as E0′, could be employed to characterize the involvement of c-type cytochromes (c-Cyts) and electron shuttles in bioelectrochemistry. It was calculated as E0′ = (Ered + Eox)/2, where Ered and Eox represent the potentials corresponding to the reduction and oxidation peaks, respectively. (41,42) Between −800 and 600 mV applied potential, the S. oneidensis@FeS system displayed one more pair of redox peaks (E2 = 220 mV vs Ag/AgCl) than S. oneidensis (E1 = −320 mV vs Ag/AgCl). In particular, E1 and E2 were attributed to the flavin/c-Cyts combination and c-Cyts, correspondingly. (43−46) The immobilized biofilm cultivation method resulted in tighter contact between the biofilm and the electrode. Therefore, it did not require flavin as an electron shuttle to mediate electron transfer as in our previous study. (11) Moreover, FeS NPs activated more electroactive proteins (c-Cyts) and engaged them in cathodic electron uptake. The respective characteristic peak currents of S. oneidensis and S. oneidensis@FeS systems progressively increased over three cycles, individually suggesting a determining function of the flavin/c-Cyts combination and the c-Cyts in the EET. Larger CV curve areas (capacitance) reflected a stronger ability to store electrons (Figure 6B,F). The capacitances of S. oneidensis and S. oneidensis@FeS systems were improved from 0.58 and 1.56 mF to 0.70 and 1.71 mF, respectively. Because of their reaction cycles (15 and 9 days), the S. oneidensis@FeS system had a significantly higher capacitance accumulation rate, which could not be achieved without more activated c-Cyts.

Figure 6

Figure 6. Electrochemical analysis in MES systems. Cyclic voltammetry curves, capacitance, Nyquist plots of electrochemical impedance spectroscopy, and the values of the Rs and Rct in (A–D) S. oneidensis and (E–H) S. oneidensis@FeS systems.

EIS was performed to analyze the microbial electrochemical system composition and the properties during electrode reactions. (47) S. oneidensis and S. oneidensis@FeS systems both displayed typical Nyquist plots, which manifested as a semicircle and a diagonal line (Figure 6C,G). Figure 6D and H illustrates that in S. oneidensis and S. oneidensis@FeS systems, the ohmic resistance (Rs) remained stable, varying from 13.8 to 13.3 Ω and from 15.9 to 14.2 Ω, correspondingly. On the other hand, their initial charge transfer resistances (Rct) were 26.8 and 5.2 Ω, attributed to the high conductivity of FeS NPs, making the charge transfer accessible and further minimizing ohmic polarization (Figure S3). The high conductivity of FeS NPs allowed the electron transfer not to be restricted by the distance within a specific range, which prevented the perishing of the outer biofilm that was difficult to obtain electron. Thus, S. oneidensis@FeS biofilms had more contact area with the cathode, which resulted in more efficient electron utilization (Figure S5). Moreover, the enhanced catalytic rate led to a reduction in activation polarization of S. oneidensis@FeS system (Figure 2C,D). (48) These reasons contributed to a higher cathode efficiency in the S. oneidensis@FeS system (Figure 4E). Naturally, a portion of the electrons was consumed due to concentration polarization and biomass maintenance and growth in both systems. (49,50) Due to the spatial structure, the limited contact area between the flexible cells and rigid solid electrodes in Shewanella bacteria limited the EET efficiency. FeS NPs activated idle electroactive proteins so as to enhance the interfacial electron transfer efficiency, which was reflected by prominent redox peaks, high capacitance, and low electron transfer resistance.

Molecular-Level Analysis for Surface Group and Electroactivity

Electrochemical in-situ Fourier transform infrared spectra revealed an external redox protein phase transition behavior involved during the EET process at the molecular level. The combined change in gradient potential and chemical band implied a redox reaction between biofilm and electrode and a protein molecular conformation transition (Figure 7). (51) At 1201, 1558, and 1683 cm–1, the intensity continuously escalated with the applied potential from −0.9 to 0.4 V, corresponding to the polarization of c-Cyts, C–N group in amide II, and C═O group in amide I, respectively. (52) As polarization intensity was proportional to the relative dielectric constant, the FeS NPs rendered S. oneidensis with more substantial electron storage capacity to participate in extracellular respiration. (53,54) This corroborated the previous remarks that the S. oneidensis@FeS system had a greater capacitance. (55) As demonstrated in our previous work, c-Cyts, as a typical electroactive protein, played an electron transfer role in reversing EET. (11) As a protein-like substance, the amide group could also act as a momentous electron transfer site first discovered in MES of ammonia. (56) It was reported that an applied electric potential could induce amide group polarization and provide a motive force for electron hopping between proteins, in which the amide group could function as a relay station for electron transfer. (57) C–N and C═O were essential active sites in protein-like substances involved in electron transfer. For example, after polarization, the electrons around the N and O atoms move away from the corresponding nuclear state and into higher energy states, which would facilitate electron transfer. In addition, C═O could accept protons to form ·C–O–H resulting in the electron transfer. (58) Consequently, the polarized amide groups and c-Cyts on the cell surface meant that more electrons in higher energy states could be transferred through protein-like substances and electroactive proteins.

Figure 7

Figure 7. Electrochemical in-situ Fourier transform infrared spectra in (A) S. oneidensis and (B) S. oneidensis@FeS systems.

Proposed Mechanism

Based on these above results, the mechanism was proposed as the following three pathways (Figure 8). Besides the proven reversed Mtr pathway (the first pathway), biological self-assembled transmembrane electron conduits (FeS NPs) could likewise transfer electrons from the extracellular to the intracellular environment, and electrons were ultimately distributed to NapA, NapB, and NrfA without CymA, resulting in the DNRA process (the second pathway). (11) Furthermore, the amide group in protein-like substances facilitated electron transfer in the outer membrane (the third pathway). Although the role of protein-like substances in S. oneidensis in electron transfer has not been explicitly stated, Okamoto et al. demonstrated that proteins distinct from the outer membrane cytochrome c complex (MtrCBA) couple proton transport with EET to maintain charge neutrality in the periplasm. (59) Considering the H+-consuming DNRA process, these proteins are similarly likely to bind proton transport in the inward EET. Nevertheless, it was necessary to investigate further whether electrons directly interacted with nitrate reductase and nitrite reductase or entered into the cellular menaquinone pool and reacted with one or more inner membrane cytochromes, permitting electrons to flow into existing electron transfer chain compositions and eventually into reductase in the periplasmic space. Moreover, due to insufficient genes coded for c-Cyts and the absence of conductive pilus-like structures, S. oneidensis exhibited deficiencies in outward and inward EET. (60) The hybrid system allowed more c-Cyts to operate, and functionally, FeS NPs were similar to type IV pili. Hence, the “bionic type IV pili” compensated for the congenital losses in S. oneidensis MR-1.

Figure 8

Figure 8. Schematic illustration of the mechanism. OmcA and MtrC, extracellular iron oxide respiratory system surface decaheme cytochrome c component; MtrB, extracellular iron oxide respiratory system outer membrane component; MtrA, extracellular iron oxide respiratory system periplasmic decaheme cytochrome c component; CymA, membrane anchored tetraheme c; MQ, menaquinone; MQH2, reduced form of menaquinone; NapB, periplasmic nitrate reductase cytochrome c subunit; NapA, periplasmic nitrate reductase molybdopterin-binding subunit; NrfA, ammonia-forming nitrite reductase.

Implications

The contradiction between chemical reaction kinetics and thermodynamics leads to an unsatisfactory energy conversion efficiency in the Haber-Bosch process (10–20%). (61) Ammonia could be synthesized sustainably and efficiently by reducing contaminant nitrate via renewable electricity as an energy source with the electrotroph S. oneidensis as a biocatalyst. For renewable electricity, the minimal theoretical energy consumption is roughly 60% of the traditional methane-based Haber–Bosch technology. (62) In 2017, the weighted average cost of renewable electricity globally dropped within the range of fossil fuels, i.e., between $0.047 and $0.167 per kWh. (63) From 2010 to 2017, utility-scale solar and onshore wind electricity prices have declined by 73 and 23% to $0.1 per kWh and $0.06 per kWh, respectively. (64) With these latest advances and the declining cost of renewable energy production, it creates opportunities for sustainable NH3 synthesis pathways to compete with the prevailing Haber–Bosch technology in future markets. Furthermore, when electricity prices fall below 4 cents per kWh and energy conversion efficiencies achieve at least 60%, electrochemical production is comparable in cost to traditional fossil fuel-derived processes. (64) However, the limited electron transfer between interfaces restricts the cathode efficiency (33.1%) and selectivity (82.5%). (11) Inspired by biomineralization, the hybrid system based on microorganisms and nanomaterials is an attractive intersection and emerging direction for biology and materials science, combining self-repair and catalytic activities, respectively. (65) Remarkable dispersion structure, high surface energy, and strong biocompatibility significantly improve the stability relative to artificial counterparts, indicating effective, economical, and sustainable application prospects. (27) Herein, the biohybrid system effectively breaks the electron transfer limitation for natural bacteria and improves the cathode efficiency and selectivity to an unprecedented maximum of 65.4 and 98.0% in MES of ammonia. In addition to S. oneidensis, sulfate-reducing bacteria lacking outer-membrane cytochromes and electron mediators could also biosynthesize FeS NPs to achieve EET, significantly improving the applicability of the biohybrid system. (66) This work may improve our comprehension of the interconnection between semiconductor materials and bacteria and contribute to exploring new EET proteins. For MES technology, which is just in its infancy in research, achieving this goal still requires continuous efforts.

Supporting Information

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The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.3c10897.

  • Photographs of biosynthesized FeS in wild-type and mutant strains; Fe(II) concentration, UV–vis-NIR absorption spectra, and electrochemical characteristics (CV, capacitance, Nyquist plots, and the values of Rs and Rct) in the optimizing biosynthesized-FeS NPs experiments; CLSM images of S. oneidensis and S. oneidensis@FeS biofilm; SEM and EDS mapping images of S. oneidensis and S. oneidensis@FeS; HAADF-STEM and EDS mapping images of the sliced mutant strains-FeS; TOC concentration in S. oneidensis, S. oneidensis@FeS, mutant strains, and mutant strains-FeS systems; schematic diagram and the composition of electrolyte solution in MES system (Figures S1–S11 and Table S1) (PDF)

Biological Self-Assembled Transmembrane Electron Conduits for High-Efficiency Ammonia Production in Microbial Electrosynthesis

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S1
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Supporting Information
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Biological self-assembled transmembrane electron conduits for high-efficiency
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ammonia production in microbial electrosynthesis
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Yao Li, Sen Qiao*, Meiwei Guo, Liying Zhang,
Guangfei Liu and Jiti Zhou
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Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education,
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China), School of Environmental Science and Technology, Dalian University of Technology,
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Dalian 116024, P.R. China
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*Corresponding author:
qscyj@mail.dlut.edu.cn
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S2
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Total pages: S1-S15
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Total figures: S3-S13
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Total tables: S14
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Contents:
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Page S3,
Figure S1
Images of FeS NPs biosynthesized by
S.oneidensis
MR-1 under different
27
incubation time.
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Page S4,
Figure S2
Optimizing FeS NPs biosynthesis. (A) Time profile of Fe(II) concentration
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in the biosynthesis-FeS. (B) UV-vis-NIR absorption spectra of biosynthesis-FeS.
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Page S5,
Figure S3
Electrochemical characteristics of FeS NPs. (A) Cyclic voltammetry curves.
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(B) Capacitance. (C) Nyquist plots of electrochemical impedance spectroscopy. (D) The value of
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the R
s
and R
ct
.
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Page S6,
Figure S4
Schematic diagram of MES system.
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Page S7,
Figure S5
CLSM images of
S. oneidensis
biofilm. (A-F) Cycle 1 and (G-L) Cycle 3,
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among them, (A)(D)(G)(J) total cells, (B)(E)(H)(K) living cells, and (C)(F)(I)(L) dead cells (scale
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bar: 100 and 200
μ
m).
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Page S8,
Figure S6
CLSM images of the
S. oneidensis
@FeS biofilm. (A-F) Cycle 1 and (G-L)
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Cycle 3, among them, (A)(D)(G)(J) total cells, (B)(E)(H)(K) living cells, and (C)(F)(I)(L) dead
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cells (scale bar: 100 and 200
μ
m).
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Page S9,
Figure S7
SEM images. (A)
S. oneidensis
. (B)-(F) EDS mapping of
S. oneidensis
(scale
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bars: 500 nm). (G)
S. oneidensis
@FeS. (H)-(L) EDS mapping of
S. oneidensis
@FeS (scale bars:
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500 nm).
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Page S10,
Figure S8
The total organic carbon (TOC) concentration in (A)
S. oneidensis
and (B)
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S. oneidensis
@FeS systems.
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Page S11,
Figure S9
Images of FeS NPs biosynthesized by
S.oneidensis
MR-1 mutants.
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Page S12,
Figure S10
Characteristics of the biosynthesis-FeS in mutants. HAADF-STEM images
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of the sliced (A)
omcA/mrtC
-FeS and (E)
cymA
-FeS. EDS mapping of the sliced (B-D)
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omcA/mrtC
-FeS and (F-H)
cymA
-FeS (scale bars: 250 nm).
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Page S13,
Figure S11
The TOC concentration in mutants.
50
Page S14,
Table S1
The composition of electrolyte solution in MES.
51

Terms & Conditions

Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Author Information

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  • Corresponding Author
  • Authors
    • Yao Li - Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    • Meiwei Guo - Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    • Liying Zhang - Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
    • Guangfei Liu - Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. ChinaOrcidhttps://orcid.org/0000-0001-9514-3271
    • Jiti Zhou - Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education, China), School of Environmental Science and Technology, Dalian University of Technology, Dalian116024, P.R. China
  • Notes
    The authors declare no competing financial interest.

Acknowledgments

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The authors deeply appreciate Prof. Kenneth Nealson (University of Southern California) for kindly providing us MR-1 and related mutant strains. This work was supported by the National Natural Science Foundation of China (No. 22176026); the National Key Research and Development Project (2019YFA0705804).

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  • Abstract

    Figure 1

    Figure 1. Characteristics of the S. oneidensis@FeS system.

    Figure 2

    Figure 2. Nitrate reduction performances in S. oneidensis and S. oneidensis@FeS systems.

    Figure 3

    Figure 3. Nitrate reduction was by different mutants. (A) NO3-N, (B) NO2-N, and (C) NH4+-N concentrations. (D) Yield assessment. Each experiment was performed in triplicate, and error bars indicate the standard deviation.

    Figure 4

    Figure 4. Cathodic electron consumption in MES systems. Current density and coulomb in (A, B) S. oneidensis and (C, D) S. oneidensis@FeS systems. (E) Cathode efficiency and (F) a comparison of achievements.

    Figure 5

    Figure 5. Cathodic electron consumption by different mutants. (A) Current density, (B) Coulomb. (C) Cathode efficiency.

    Figure 6

    Figure 6. Electrochemical analysis in MES systems. Cyclic voltammetry curves, capacitance, Nyquist plots of electrochemical impedance spectroscopy, and the values of the Rs and Rct in (A–D) S. oneidensis and (E–H) S. oneidensis@FeS systems.

    Figure 7

    Figure 7. Electrochemical in-situ Fourier transform infrared spectra in (A) S. oneidensis and (B) S. oneidensis@FeS systems.

    Figure 8

    Figure 8. Schematic illustration of the mechanism. OmcA and MtrC, extracellular iron oxide respiratory system surface decaheme cytochrome c component; MtrB, extracellular iron oxide respiratory system outer membrane component; MtrA, extracellular iron oxide respiratory system periplasmic decaheme cytochrome c component; CymA, membrane anchored tetraheme c; MQ, menaquinone; MQH2, reduced form of menaquinone; NapB, periplasmic nitrate reductase cytochrome c subunit; NapA, periplasmic nitrate reductase molybdopterin-binding subunit; NrfA, ammonia-forming nitrite reductase.

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  • Supporting Information

    Supporting Information


    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.est.3c10897.

    • Photographs of biosynthesized FeS in wild-type and mutant strains; Fe(II) concentration, UV–vis-NIR absorption spectra, and electrochemical characteristics (CV, capacitance, Nyquist plots, and the values of Rs and Rct) in the optimizing biosynthesized-FeS NPs experiments; CLSM images of S. oneidensis and S. oneidensis@FeS biofilm; SEM and EDS mapping images of S. oneidensis and S. oneidensis@FeS; HAADF-STEM and EDS mapping images of the sliced mutant strains-FeS; TOC concentration in S. oneidensis, S. oneidensis@FeS, mutant strains, and mutant strains-FeS systems; schematic diagram and the composition of electrolyte solution in MES system (Figures S1–S11 and Table S1) (PDF)


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