Enhanced Bioelectrocatalysis of Shewanella oneidensis MR-1 by a

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Enhanced Bioelectrocatalysis of Shewanella oneidensis MR-1 by a Naphthoquinone Redox Polymer Kamrul Hasan, Matteo Grattieri, Tao Wang, Ross D. Milton, and Shelley D. Minteer ACS Energy Lett., Just Accepted Manuscript • DOI: 10.1021/acsenergylett.7b00585 • Publication Date (Web): 31 Jul 2017 Downloaded from http://pubs.acs.org on August 1, 2017

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ACS Energy Letters

Enhanced Bioelectrocatalysis of Shewanella oneidensis MR-1 by a Naphthoquinone Redox Polymer Kamrul Hasan, Matteo Grattieri, Tao Wang, Ross D. Milton and Shelley D. Minteer* Departments of Chemistry and Materials Science & Engineering, University of Utah, Salt Lake City, UT 84112, United States Abstract Shewanella oneidensis MR-1 is the model organism used in microbial fuel cells (MFCs). A great deal of research has focused on this bacterium to improve their extracellular electron transfer (EET) and subsequently the power output in MFCs. Here, we report on the enhanced bioelectrocatalysis of S. oneidensis MR-1 by using a naphthoquinone redox polymer (NQ-LPEI) on a modified carbon felt electrode. A maximum anodic current of 3.70 ± 0.40 A m-2 is obtained in a three-electrode setup, a value fifteen-times higher than that obtained for an anode that did not contain the NQ-LPEI redox polymer (0.24 ± 0.05 A m-2). Additionally, a maximum power output of 0.53 ± 0.02 Wm-2 was obtained in single chamber MFCs where the NQ-LPEI modified anode was utilized. The power output was significantly higher than that obtained for MFCs with unmodified anodes (0.19±0.05 Wm-2). These findings suggest that NQ-LPEI could be used with known electrogenic microorganisms to further improve the performances of MFCs.

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The possibility of extracting electrons from the energy metabolism of microorganisms is the foundation of microbial electrochemical systems (MESs) and could be used in many biotechnological applications, e.g., renewable energy generation, wastewater treatment, biosensing1, bioremediation, production of valuable biochemical,s etc2-3. One widely studied example of MESs is the microbial fuel cell (MFC) where heterotrophic microorganisms are used to convert organic substrates/fuels into electrical power at high effiencies4. Although a great deal of research was devoted to studying this technology, no economically viable industrial application has yet to be achieved due to their limited power output and instability compared to the traditional precious-metal catalyzed fuel cell. Nevertheless, MFCs have great advantages due to the self-sustainable nature of microorganisms which can use a wide range of fuels and the possibility to produce valuable chemicals as products, i.e., hydrogen, formate, acetate, methane, etc5.


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One of the key challenges of MFCs is extracellular-ET (EET)2 to/from microorganisms, since their cell envelope is neither electrically conductive nor physically permeable to minerals surrounding them. However, certain microorganisms, called exoelectrogens (or electroactive bacteria), are competent to exchange electrons to metals adjacent to them. EET occurs mainly by two ways, either direct electron transfer (DET) or mediated electron transfer (MET). A direct interaction between the microbial cell membrane and a solid-state electron acceptor is required for DET. Membrane bound redox proteins or outer membrane cytochromes (OMCs) are also accountable for DET2. Shewanella oneidensis MR-1 is a gram-negative, metabolically versatile dissimilatory metalreducing bacterium. It is one of the most widely studied bacterium in MESs due to its capability to form electrically conductive biofilms which comprise cells and extracellular substances6. For EET, S. oneidensis MR-1 uses their metal reducing (Mtr) pathway to transfer electrons (via ctype cytochromes) from the quinone-pool inside the cytoplasmic membrane, through the periplasmic space and across the outer membrane (via Mtr proteins and OMCs). Under O2 limited condition, S. oneidensis was reported to generate conductive pili, often referred as nanowires (an extension of outer membrane and periplasm) for distant ET via a multistep electron hopping mechanism7-9. Additionally, some small redox active molecules for example, quinone derivatives and flavins10 can act as diffusive electron shuttles for self-excreted DET. Recently, the mechanistic EET model of S. oneidensis MR-1 was reviewed by Leech et al11. However, the detailed mechanism, complexity and the physiology of ET from the central metabolism to electrode surfaces is not clearly understood12. Although DET is preferable in MFCs, the electrical current and power output generated from a DET-based systems is usually lower (due to sluggish ET rates) than that of a MET-based system13.


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To improve EET from microorganisms, substantial research was dedicated mostly to engineering microorganisms14 and developing new advanced materials15 as well as configurations and prototypes of MFCs5. In a single chamber MFC constructed with carbon fiber brush anode and Pt cathode, the maximum power of 0.332 ±0.021 W m-2 was reported with pure culture of S. oneidensis MR-116. On carbon nanotubes and polyaniline modified macroporous graphite felt, S. putrfaciens was able generate 0.308 W m-2 17. The power output was shown to improve at 0.693±0.036 Wm-2 on an inkjet-printed polyaniline modified carbon paper electrode18. In a ‘straw hydrolysate MFC’ constructed with polyaniline modified carbon cloth in combination with riboflavin addition, pure cultures of S. oneidensis MR-1 produced 0.66 Wm-2 19

. Recently Zou et a., reported the maximum power at 1.28 Wm-2 in a double chamber MFC

equipped with polyaniline hybridized mesoporous carbon anode20. In a double chamber MFC constructed with ionic liquid functionalized graphene nanosheets, S. oneidensis MR-1 was reported to generate 0.601 Wm-2 21. In these studies, a double chamber MFC setup was frequently used that requires a highly expensive proton exchange membrane. In addition to that, advanced electrode materials were used as the anode and Pt was often used as the cathode. Large scale fabrication of these anode materials is complicated and Pt is very expensive. Also, ferricyanide was often used as a catholyte in those system that is considered as an environmental toxic agent. Considering these issues, double chamber construction and use of Pt makes MFCs expensive and has hindered their large-scale industrial application, especially for wastewater treatment. In MET-based systems, an exogenous ET-mediator is required to reversibly diffuse through the microbial respiratory system to transfer electrons to electrodes. Using such exogenous ETmediators (typically quinone derivatives) is technologically unfeasible, environmentally


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unfriendly, practically incompatible and may be harmful for the environment13. Instead, surface confined polymeric mediators can act as an immobilization matrix for microbial cells as well as an ET-mediator. They can form three-dimensional (3D) structures around biocatalysts on electrode surfaces (do not diffuse into the bulk solution) and subsequently improve rates of bioelectrocatalysis22. Osmium-based redox polymers were extensively studied to electrically wire a series of bacterial cells23-24, yeast cells25 and also photosynthetic organisms26. Previously an osmium redox polymer with a relatively positive formal potential (E0’ = +0.176 V vs. SCE) was investigated to enhance the EET from S. oneidensis MR-124. However, the significantly higher positive formal potentials of this polymer lead to voltage losses due to the potential difference between the active site of the biomaterials and the electron mediators. Thus, the use of this kind of polymer for practical applications in MFCs is limited. Instead naphthoquinone derivatives, for instance vitamin K, play an important role in biological ET systems27. Naphthoquinone (NQ) based redox polymers having negative formal potentials (E0’) were demonstrated as an alternative ET-mediator in enzymatic bioelectrocatalysis28. The use of NQ-based polymers is rapidly increasing for glucose oxidizing enzymes, since their E0’ can be tuned to support the local ET-environment29. However, NQ-LPEI has never been investigated as a ET-mediator with S. oneidensis MR-1 to improve their EET. Here we investigated the use of NQ-LPEI to improve the bioelectrocatalysis of S. oneidensis MR-1 on carbon felt electrodes. The efficiency of NQ-LPEI is evaluated in a single chamber MFC, where carbon felt electrodes were used as the anode and activated carbon-based electrodes were used as the cathode (air breathing). In this communication, we consider DET to be the case where exogenous ET-mediators are not


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included to establish ET, thus, we consider the use of a redox polymer, (in this case, NQ-LPEI) to be MET. S. oneidensis MR-1 is well known for its ability to undergo DET with electrodes11. To investigate their DET competences on carbon felt electrodes, cells grown in M1 medium were harvested and suspended in the electrochemical cell. Cyclic voltammograms were performed under non-turnover (bioelectrocatalysis with substrate deprived conditions) and under turnover conditions (bioelectrocatalytic substrate consumption), as shown in Figure 1. To obtain a potential controlled bioelectrocatalytic current, the working electrode was polarized at 0 V vs. SCE for 18.5 days until the catalytic current reached an apparent steady-state at 0.24 ± 0.05 A m2

(Figure 1, inset). At this point, turnover cyclic voltammograms were recorded where a

reductive peak appears at -0.25 V and an oxidative peak appears at -0.03 V (Figure 1, red line). Thus, their formal potential, E0’ [(-0.25 V -0.03 V)/2] is determined at -0.14 V, which is attributed to the c-type outer membrane cytochrome (Cyt c). This E0’ is consistent with the value reported earlier for Cyt c30. Under these turnover CV conditions, the catalytic onset potential was determined to be approximately -0.34 V, being coherent with a E0’ for metal reducing c-type cytochrome (MtrC)30. In the literature, the E0’ of Cyt c differ broadly due to the experimental variation such as electrode material (i.e. either causing Cyt c to be surface confined or soluble in the electrolyte) and the pH gradient at the electrode surface31. In addition to the cytochromes, pili and flavin32 can also play a role for EET from the bacterial cells to the electrode. Moreover, pili are also attributed for bacterial cell attachment on the electrode surface and subsequently biofilm formation11.


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Figure 1. Representative cyclic voltammograms of S. oneidensis MR-1 on bare carbon felt (no NQ-LPEI modification) under non-turnover and turnover conditions performed after 18.5 days of polarization at 0 V. Substrate: 18 mM Lactate, Scan rate: 2 mV s-1. Inset shows the amperometric i-t curve on bioelectrocatalysis of S. oneidensis MR-1 on a bare carbon felt electrode. Applied potential (Eapp) = 0.0 V vs. SCE. To facilitate the EET of S. oneidensis MR-1, carbon felt was modified with the NQ-LPEI redox polymer. For this, 100 µL of a solution mixture containing NQ-LPEI and ethylene glycol diglycidyl ether (EGDGE) was evenly distributed on the electrode surface and allowed to dry at room temperature (20 ± 2 °C). EGDGE was used to crosslink the NQ-LPEI on the electrode surface. The ratio of NQ-LPEI and EGDGE was optimized at 21 µL:1.13 µL according to a previously published report33. CVs were performed on a bare carbon felt electrode as well as on a NQ-LPEI modified electrode in the absence of S. oneidensis MR-1 to confirm the modification of the carbon felt surface with the redox polymer (Supporting information, Figure S1). The cyclic voltammogram of the NQ-LPEI modified electrode displays a pair of redox peaks at -0.33 V (Figure S1) that is consistent with the theoretical E0’ reported earlier for this polymer28. An


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additional pair of redox peaks appears at -0.24 V, which is in agreement with the previous report that shows the peaks represent a side product developed during the polymer synthesis28. To evaluate MET from S. oneidensis MR-1 on NQ- LPEI modified electrodes, harvested cells were suspended in the electrochemical cell containing M1 medium (as an electrolyte) to allow natural electrochemical growth. Previously this approach of microbial inoculation was shown to yield greater bioelectrocatalysis compared to a situation where microbial cells were directly immobilized within a polymer coated electrode for other polymers24. Cyclic voltammograms were conducted under non-turnover and turnover conditions after running a long chronoamperometric experiment for 113 h (Figure 2 A). The sigmoidal shape of the turnover cyclic voltammograms with two distinguished waves at -0.3 V and -0.2 V correspond to the two characteristic redox peaks for NQ-LPEI (Figure S1). The sigmoidal shape of the cyclic voltammograms at low scan rate (1-2 mV s-1) indicates the electrochemical redox transition coupled to a redox reaction34. These data confirm the bioelectrocatalytic electrons generated from S. oneidensis MR-1 are mediated by the naphthoquinone redox centers embedded in the polymer matrix. The chronoamperometric plot on both bare carbon felt (black line) and on NQ-LPEI modified carbon felt (red line) is presented in Figure 2B. The catalytic response on a bare carbon felt electrode is about 0.030±0.005 Am-2 at 113 h. This low current generation is attributed to slow DET of S. oneidensis MR-1 that requires the long adaptation time for bacterial cells to attach on the electrode surface. This inoculation time (113 h) fit under the long startup period (≈ 3 days) detected with unmodified carbon electrode (Figure 1, inset). Instead, on NQ-LPEI modified electrodes, the startup time for current generation is much faster (≈ 5 h) than that of the unmodified electrode. The shorter startup time is accredited to the enhanced electrochemical


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communication and ET mediated by the NQ-LPEI. By amperometric i-t analysis, the maximum bioelectrocatalytic current was recorded to be 3.7 ± 0.4 A m-2 (Figure 2B), at approximately fifteen times higher than the current obtained for DET (Figure 1, inset). The improved bioelectrocatalytic current may also corresponds to the better cell attachment and electroactive biofilm formation on the electrode surface. Scanning electron micrographs (SEMs) of bare carbon felt, an electroactive biofilm on a bare carbon felt and an NQ-LPEI modified carbon felt is presented in Figure S2.

Figure 2. A) Representative cyclic voltammograms of S. oneidensis MR-1 on NQ-LPEI modified carbon felt at non-turnover (black line) and turnover condition (red line) performed after 112.5 h of chronoamperometric experiment (Inset shows the chemical structure of NQLPEI). B) Chronoamperometric i-t curve for catalytic current generation on carbon felt electrode


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(black line) and on NQ-LPEI modified carbon felt (red line) as a function of time from innoculation. Applied potential (Eapp) = 0.0 V vs. SCE. Substrate: 18 mM Lactate, Scan rate: 2 mV s-1. In addition to carbon felt electrodes, enhanced bioelectrocatalysis of S. oneidensis MR-1 was also obtained on NQ-LPEI modified Toray carbon paper electrodes (Figure S3). To investigate the outcome of NQ-LPEI itself under non-turnover and turnover conditions, cyclic voltammograms were conducted on polymer modified Toray carbon paper electrodes in the absence of microbial inoculation. As shown in Figure S4, the characteristic redox peaks of the redox polymer under turnover conditions are slightly decreased compared to the non-turnover conditions. Additionally, bioelectrocatalysis was not observed in the absence of bacterial cells as expected. The lower peak currents under turnover conditions is most likely attributed to some delamination of the redox polymer from the electrode surface over the long chronoamperometric experiment (112.5 h). These data indicate that the enhanced bioelectrocatalytic current obtained in Figure 2 is obtained by the electron mediating properties of the NQ-LPEI. Previously, osmium redox polymers were reported for electrical wiring of a gram-positive bacterium (Bacillus subtilis) having a thick cell wall (≈ 35 nm) made of peptidoglycan and teichoic acids. It was demonstrated that it is not a prerequisite for polymeric mediators to pass through the cytosolic membrane to make efficient electronic communication; however, the entire mechanism is yet to be studied35. The evolution of the difference of potential between the anode and the cathode of MFCs equipped with NQ-LPEI modified anodes (black) and with bare carbon felt anodes (red) is reported in Figure 3. After approximately one day of operation, both the MFCs equipped with NQ-LPEI and unmodified-anodes developed a difference of potential between the electrodes.


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However, the MFCs equipped with NQ-LPEI modified anodes achieved a greater potential difference throughout this investigation (90 ± 20 mV at day 2, 190 ± 60 mV at day 5 and 240 ± 30 mV at day 10) compared to the MFCs equipped with unmodified anodes (15 ± 3 mV at day 2, 80 ± 20 at day 5 and 130 ± 50 at day 10). These results indicate that the NQ-LPEI redox polymer decreased the time necessary to establish successful EET between bacterial cells and electrode surfaces, maintaining a remarkable difference of potential between anodes and cathodes when the 1 kΩ load was applied. Moreover, the duration of degradation cycles (time between different additions of fresh substrate in the MFCs) was decreased when NQ-LPEI modified anodes were utilized, with positive effects on the time required to oxidize the organics present in solution.

Figure 3. Evolution of the difference of potential between anode and cathode for the MFCs with NQ-LPEI modified anodes (black) and for MFCs with unmodified anodes (red). Black and red arrows indicate addition of substrate to the electrolyte of MFCs with NQ-LPEI modified anodes and for MFCs with unmodified anodes respectively. The power curves obtained for the MFCs equipped with NQ-LPEI modified anodes (blue) and with bare carbon felt anodes (red) are reported in Figure 4. It can be easily noticed that the redox


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polymer modified anode allowed us to achieve a considerably higher power density (0.53±0.02 W m-2) compared to the MFCs with unmodified anodes (0.19±0.05 W m-2). These results are consistent with the improved current generation obtained for the MET system utilizing the threeelectrode setup (Figure 2B). Moreover, the current density at the maximum power was 1.7 ±0.1 Am-2 for the MFCs equipped with NQ-LPEI modified anodes and 0.6±0.2 Am-2 for the MFCs equipped with unmodified anodes. It has to be considered that, in the current experiments, bacterial cells were not immobilized on the electrode surface and the incubation time for the cell growth utilized for inoculation of the electrochemical cells and MFCs was constant. This experimental setup avoided erroneous evaluation of the bioelectrocatalytic performance due to different cell loadings on the anodes. Moreover, the contribution of the NQ-LPEI to the outstanding performances of the MFCs was confirmed by anodic quasi-stationary polarizations performed on the anodes of the MFCs (Figure S5) at two different days (day 6 and day 10). The increased current densities obtained for the NQ-LPEI anodes of the MFCs showed that the MET systems dramatically facilitated the EET, improving the performances of the full device.

Figure 4. Power curves obtained at day 10 for the MFCs with NQ-LPEI modified anodes (blue line) and for MFCs with unmodified anodes (red line).


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Here, we demonstrated significantly greater bioelectrocatalytic current generation of S. oneidensis MR-1 on naphthoquinone redox polymer (NQ-LPEI) modified carbon felt electrode versus unmodified carbon felt. NQ-LPEI is shown to facilitates the shorter start-up time for bacterial cell colonization, enhanced electrochemical communication and faster substrate degradation and subsequently greater bioelectrocatalysis. The maximum current density generation was recorded at 3.7 ± 0.4 A m-2. The greatest power output in the single chamber microbial fuel cells was documented at 0.53 ± 0.02 Wm-2. These are the maximum current generation and power output (catalyzed by pure culture of S. oneidensis MR-1) in a single chamber MFC constructed with a cost-effective anode and cathode based on Pt-free carbon materials. These findings could have significant implications to further improve the performance of microbial fuel cell with 3D macroporous electrode materials36. ASSOCIATED CONTENT Supporting Information is available. Details of experimental procedures, cyclic voltammograms of carbon felt electrode in the absence and presence of NQ-LPEI, scanning electron micrographs of bare carbon felt, electroactive biofilm on bare carbon felt and NQ-LPEI modified carbon felt, bioelectrocatalysis of S. oneidensis MR-1 on Toray carbon paper electrode and anodic quasi-stationary polarizations for NQ-LPEI modified anodes. AUTHOR INFORMATION Corresponding Author *E-mail: [email protected]


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Notes The authors declare no competing financial interest. ACKNOWLEDGMENT The authors would like to thank the USDA NIFA program for funding.

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Polyaniline Hybridized Large-Mesoporous Carbon Anode For High-Performance Microbial Fuel Cells. Electrochim. Acta. 2017, 229, 31-38. (21) Zhao, C.; Wang, Y.; Shi, F.; Zhang, J.; Zhu, J.-J. High Biocurrent Generation In Shewanella-Inoculated Microbial Fuel Cells Using Ionic Liquid Functionalized Graphene Nanosheets As An Anode. Chem. Commun. 2013, 49, 6668-6670 (22) Heller, A. Electron-Conducting Redox Hydrogels: Design, Characteristics And Synthesis. Curr. Opin. Chem. Biol. 2006, 10, 664-672 (23) Hasan, K.; Patil, S. A.; Leech, D.; Hägerhäll, C.; Gorton, L. Electrochemical Communication Between Microbial Cells And Electrodes Via Osmium Redox Systems. Biochem. Soc. Trans. 2012, 40, 1330-1335. (24) Patil, S. A.; Hasan, K.; Leech, D.; Hägerhäll, C.; Gorton, L. Improved Microbial Electrocatalysis With Osmium Polymer Modified Electrodes. Chem. Commun. 2012, 48, 10183-10185. (25) Shkil, H.; Schulte, A.; Guschin, D. A.; Schuhmann, W. Electron Transfer Between Genetically Modified Hansenula Polymorpha Yeast Cells And Electrode Surfaces Via OsComplex Modified Redox Polymers. ChemPhysChem 2011, 12, 806-813 (26) Hasan, K.; Çevik, E.; Sperling, E.; Packer, M. A.; Leech, D.; Gorton, L. Photoelectrochemical Wiring Of Paulschulzia Pseudovolvox (Algae) To Osmium Polymer Modified Electrodes For Harnessing Solar Energy. Adv. Energy Mater. 2015, 5, 1501100. (27) Lovern, D.; Marbois, B. Does Menaquinone Participate In Brain Astrocyte Electron Transport? Med. hypotheses 2013, 81, 587-591.


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(28) Milton, R. D.; Hickey, D. P.; Abdellaoui, S.; Lim, K.; Wu, F.; Tan, B.; Minteer, S. D. Rational Design Of Quinones For High Power Density Biofuel Cells. Chem. Sci. 2015, 6, 4867-4875. (29) Giroud, F.; Milton, R. D.; Tan, B.-X.; Minteer, S. D. Simplifying Enzymatic Biofuel Cells: Immobilized Naphthoquinone As A Biocathodic Orientational Moiety And Bioanodic Electron Mediator. ACS Catal. 2015, 5, 1240-1244. (30) Carmona-Martinez, A. A.; Harnisch, F.; Fitzgerald, L. A.; Biffinger, J. C.; Ringeisen, B. R.; Schröder, U. Cyclic Voltammetric Analysis Of The Electron Transfer Of Shewanella oneidensis

MR-1

And

Nanofilament

And

Cytochrome

Knock-Out

Mutants.

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(34) Katuri, K. P.; Rengaraj, S.; Kavanagh, P.; O’Flaherty, V.; Leech, D. Charge Transport Through Geobacter Sulfurreducens Biofilms Grown On Graphite Rods. Langmuir 2012, 28, 7904-7913. (35) Coman, V.; Gustavsson, T.; Finkelsteinas, A.; von Wachenfeldt, C.; Hägerhäll, C.; Gorton, L. Electrical Wiring Of Live, Metabolically Enhanced Bacillus Subtilis Cells With Flexible Osmium-Redox Polymers. J. Amer. Chem. Soc. 2009, 131, 16171-16176. (36) Yu, Y.-Y.; Zhai, D.-D.; Si, R.-W.; Sun, J.-Z.; Liu, X.; Yong, Y.-C. Three-Dimensional Electrodes For High-Performance Bioelectrochemical Systems. Int. J. Mol. Sci. 2017, 18, 90.


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Enhanced Bioelectrocatalysis of Shewanella oneidensis MR-1 by a

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