Carbon Paste Paper Anode for Microbial Fuel Cells - ACS Publications

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Extracellular Electron Transfer on Sticky Paper Electrodes: Carbon Paste Paper Anode for Microbial Fuel Cells Peter Lamberg, and Kara L. Bren ACS Energy Lett., Just Accepted Manuscript • DOI: 10.1021/acsenergylett.6b00435 • Publication Date (Web): 07 Oct 2016 Downloaded from http://pubs.acs.org on October 9, 2016

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ACS Energy Letters

Extracellular Electron Transfer on Sticky Paper Electrodes: Carbon Paste Paper Anode for Microbial Fuel Cells Peter Lamberg and Kara L. Bren* Department of Chemistry, University of Rochester, Rochester New York 14627-0216, United States AUTHOR INFORMATION Kara L. Bren [email protected]

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ABSTRACT Carbon paste paper electrodes (CPPEs) were fabricated by coating a regular paper strip with carbon paste made from graphite powder and mineral oil, followed by coating with polyaniline. The CPPEs were evaluated as anodes in bioelectrochemical cells (BECs) using Shewanella oneidensis MR-1 as bacteria that donate electrons through extracellular electron transfer. The CPPE was compared to a carbon felt electrode (CFE) modified with polyaniline under the same conditions. The BEC using the CPPE anode produces current continuously for at least 4 days without the need for additional fuel (lactate). Twenty-four hours after inoculation, the BEC using the CPPE anode generates a current density more than two times greater than the cell using the CFE, with a competitive maximum value of 2.2 A m-2. The simple fabrication, ease of modification, and low cost of the CPPE makes it a promising new bioelectrode material for microbial fuel cells.

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Microbial fuel cells (MFCs) are living systems in which bacteria consume a fuel, including substances found in wastewater, and oxidize or reduce electrodes by extracellular electron transfer (EET), converting chemical energy to electrical energy.1-3 A significant limitation in the development and use of MFCs is the requirement of low-cost anodes that are effective substrates for bacterial growth and that facilitate EET.4-6 Thus, much effort has been directed towards developing biocompatible electrode materials.7-10 Because of their high biocompatibility and low materials cost, carbon-based electrode materials are used in most MFC designs.4 Carbon paste is an example of a carbon electrode material that is simple and inexpensive to prepare, and is a common electrode modification in electrical biosensors.11 However, we have found only one instance of carbon paste being used in MFCs, in which it was applied to carbon cloth.12

Here, we demonstrate the use of a carbon paste coated paper electrode (CPPE) as an anode in a bioelectrochemical cell (BEC) with the electrogenic bacterium Shewanella oneidensis MR-1 (SO)13 providing electrons to the anode (Figure 1). The CPPE is prepared by simple application of carbon paste to paper, followed by coating with polyaniline (PANI), which is known to enhance electrode conductivity in bioelectrochemical systems.14, 15 Currents and potentials were recorded continuously for four days for SO feeding on 20 mM lactate in minimal medium (MM). EET was evaluated with cyclic voltammetry (CV) and polarization curves. A platinum wire was used as a counter-electrode (cathode) and an AgCl / saturated KCl electrode served as the reference electrode. Biofilm formation and electrode topography were evaluated by scanning electron microscopy.


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Figure 1. Schematic illustration of the BEC setup used herein. The CPPE anode is a prepared using a layer-by-layer procedure where paper is coated with carbon paste, which is then coated with a conducting polymer. Bacteria form a biofilm on the anode (bioanode) that consumes nutrients and transfers electrons to the bioanode. A platinum wire is added to close the circuit.

SO has two general pathways for EET: direct and mediated.16, 17 EET has also been proposed to occur through nanowires.18 During respiration, electrons are transferred through the Mtr complex to outer membrane cytochromes.19 The direct pathway of EET involves the transfer of electrons from outer membrane cytochromes (MtrC, OmcA) to the electrode, and has a peak current ~0.2 to 0.3 V vs. NHE; it has been suggested that bacterial metabolism limits the current at higher potentials.20-22 The mediated pathway utilizes excreted flavins as electron carriers from the Mtr complex to the electrode.23 This pathway has been assigned a potential between −0.1 to 0.2 V.24 However, the EET mechanism is still under debate. Most likely SO uses a combination of EET pathways to reduce the electrode.


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In our BEC, EET by the SO biofilm was investigated using cyclic voltammograms (CVs) between −0.3 to 0.7 or 0.8 V (Figure 2a,b). The onset potential of the major peak in the CVs using the CPPE and carbon felt electrode (CFE) is ~0.2 V. These onset potentials are comparable to the onset potentials for direct electron transfer processes in previous MFC designs using SO.2527

The major difference in the CVs between the two anode materials here is the broader peak(s)

for the CPPE.

Figure 2. Average (n=3) potential scanning measurements of BEC anodes 24 h after inoculation with SO with an applied potential of 0.4 V vs. NHE in MM with 20 mM lactate. The measurements are taken from the second scan at 10 mV s-1. a) CVs of the CFE with (solid line) and without bacteria and lactate (dotted line). b) CVs of the CPPE with (solid line) and without bacteria and lactate (dotted line).


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Polarization curves reveal that the current peaks between 0.4 – 0.5 V, and 0.4 V has been used in constant potential studies in MFCs using SO (Figure 3).21, 27, 28 By comparing the polarization curves, different peak potentials are seen for the system with the CPPE and the CFE (Figure 3a). While the CFE has its peak at ~0.4 V, the CPPE has a peak at ~0.5 V as well as a higher current at its peak potential. If a CV shows a broader, flatter and more negative reductive peak, it can generally be attributed to decreased electrode conductivity. However, the fact that the CVs using the CPPE have both higher currents and several additional peaks compared to the CVs using the CFE indicates that additional reductive processes are detected for the system using the CPPE.

Current production by the biofilm at a poised potential 0.4 V was monitored for four days (see Supporting Information, section 3.2 for details). The CPPE generates a current density (146 ± 13 mA m-2) similar to the CFE (155 ± 11 mA m-2) under these conditions (Figure 3b). A similar current density vs. time curve was seen during the four days of measurement for both electrode types. Additionally, to test stability, CPPEs were left in the BEC compartment for a week. These showed no visible degradation and maintained ~20% current density despite no addition of nutrients (Figure S1).


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Figure 3. a) Average (n=3) polarization curves of a 24-hour biofilm of CPPE (red) and CFE (blue). b) Monitoring average (n=3) biofilm current generation in BEC with CPPE and CFE anodes. Currents are subtracted with baselines, e.g., BECs without SO or lactate. Electrodes were poised at 0.4 V for four days, stopping for other electrochemical evaluations every 24 h.

Figure 4a shows typical fibers of the CFE imaged by a field emission scanning electron microscope (FESEM). Comparing to the surface of the CPPE (Figure 4d), higher porosity can be seen in the network of CFE fibers, which would give the CFE higher surface area, even though the electrodes have similar macroscopic areas. The deposited biofilm 24 h after inoculation is shown in Figure 4c,f. SO formed interconnected colonies on CFE, bridging individual fibers in a dense and cohesive biofilm (Figure 4c). On the CPPE the biofilm was scattered into islands of


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embedded colonies (Figure 4f). More detailed images of the SO biofilms can also be seen in Supporting Information, Figure S3.

PANI was found to be a vital component to enhance both performance and stability of CPPE and CFE. Studies done on non-coated anodes showed poor electrical signals in BECs with a CFE and lowered currents in BECs with a CPPE (Figure S2). PANI is expected to decrease surface hydrophobicity, facilitating interactions of water-soluble mediators and cytochromes. Deposits of PANI can be seen in FESEM images on both CFE and CPPEs after treatment (Figure 4b and e).


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Figure 4. FESEM images of a) CFE without PANI coating, b) CFE surface, c) CFE with a 24 h biofilm of SO, d) CPPE without PANI coating, e) CPPE surface, f) CPPE with a 24 h biofilm of SO. Images were taken at 2k magnification with an accelerating voltage of 20 kV. Scale bars are set to 2 µm.

In an MFC the maximum current density will depend on the electrical connection and compatibility between the bacteria and electrode interface, making electrode design critical.29 Developing new electrodes for MFCs thus has been a key strategy for enhancing performance. Most other carbon-based electrode designs have reported maximum current densities measured for lactate MFCs with SO in the range of 1 – 20 A m-2,30 and our CPPE falls within this range (Table 1). Optimal potential is considered to be the peak potential seen in the polarization curves, and the maximum current density is calculated using the generated current at the peak potential. Considering that our BEC is not optimized for producing maximum possible current density, or for the optimal potential of the CPPE, further development of the CPPE may eventually yield current densities in the upper range.

Table 1. Comparison of averaged experimental data obtained from polarization curves after 24 h incubation for both electrodes (n=3). Electrode type Maximum current density (A m-2) Optimal potential (V)

CPPE

CFE

2.24 ±0.16

0.94 ±0.09

0.52

0.41


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Our study reports a simple and inexpensive paper-based electrode for use as an anode in a BEC with SO. The maximum current output seen in our BEC using a CPPE anode at an applied potential of 0.4 V vs NHE was 146 ± 13 mA m-2, compared to 155 ± 11 mA m-2 for a CFE anode. However, according to polarization curves, the CPPE anode would exhibit maximum current densities of up to 2.24 ± 0.16 W m-2 without diffusion limitation, more than two times higher than the CFE, and rivaling many other electrodes conventionally used in MFCs.30 The ease of fabrication, low cost, and biocompatibility of CPPEs make them attractive electrodes for use in MFCs. Furthermore, the ease with which they may be modified will enable many possible directions for future study and application.

EXPERIMENTAL METHODS CPPEs were manufactured in lab using conducting grade graphite powder -200 mesh, UCP-2 grade 99.9995% (Alfa Aesar, Haverhill, MA USA), heavy mineral oil (Thermo Fischer, Waltham, MA USA) and strips of paper (Staples copy paper, 92 US bright, 75 g m-2, non-acid) (Figure 1). The carbon paste was made by mixing graphite powder with heavy mineral oil at a ratio of 70:30 (w/w), which was previously shown to yield a material with optimal conductance.31 The paste was applied in a ~0.5 – 1.0 mm thick layer on both sides of a 0.5 x 1.0 cm strip of paper and was hand-pressed between two sheets of aluminum foil. For comparison to the CPPE, an electrode constructed of a conventional material, carbon felt (1.3 cm thickness, 95%, Alfa Aesar), was also cut into in 0.5 x 1.0 cm strips with 0.4 cm thickness. The CFE and the CPPE were coated with PANI to enhance stability and increase conductivity, see Supporting Information section 3.2.


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The CPPE or the CFE was fixed to the electrode holder of the BEC by using a copper wire, and wrapped with Parafilm to cover the wire (approximate geometrical area of 1.0 cm2 for CPPE, 1.5 cm2 for CFE). The electrodes were stored in a dry atmosphere until they were installed in the BEC. Details on BEC construction, cell culturing, electrochemical methods, and electron microscopy can be found in Supporting Information.

ASSOCIATED CONTENT Contents of Supporting Information: Additional electrochemical tests, high magnification scanning electron microscopy imaging, Experimental details.

AUTHOR INFORMATION [email protected]

Notes The authors declare no competing financial interest

ACKNOWLEDGMENT The authors acknowledge financial support from NSF CHE-1409929 and the University of Rochester Materials Science Program. The authors are grateful to Brian McIntyre for FESEM imaging, Jeff Gralnick for the gift of SO, and Sanela Lampa-Pastirk for assistance with SO handling.

REFERENCES


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(27) Wu, C.; Cheng, Y.-Y.; Li, B.-B.; Li, W.-W.; Li, D.-B.; Yu, H.-Q. Electron Acceptor Dependence of Electron Shuttle Secretion and Extracellular Electron Transfer by Shewanella oneidensis MR-1. Bioresource Technol. 2013, 136, 711-714. (28) Wang, V. B.; Kirchhofer, N. D.; Chen, X.; Tan, M. Y. L.; Sivakumar, K.; Cao, B.; Zhang, Q.; Kjelleberg, S.; Bazan, G. C.; Loo, S. C. J., et al. Comparison of Flavins and a Conjugated Oligoelectrolyte in Stimulating Extracellular Electron Transport from Shewanella oneidensis MR-1. Electrochem. Commun. 2014, 41, 55-58. (29) Cornejo, J. A.; Lopez, C.; Babanova, S.; Santoro, C.; Artyushkova, K.; Ista, L.; Schuler, A. J.; Atanassov, P. Surface Modification for Enhanced Biofilm Formation and Electron Transport in Shewanella Anodes. J. Electrochem. Soc. 2015, 162, H597-H603. (30) Xie, X.; Criddle, C.; Cui, Y. Design and fabrication of bioelectrodes for microbial bioelectrochemical systems. Energ. Environ. Sci. 2015, 8, 3418-3441. (31) Valentini, F.; Amine, A.; Orlanducci, S.; Terranova, M. L.; Palleschi, G. Carbon Nanotube Purification: Preparation and Characterization of Carbon Nanotube Paste Electrodes. Anal. Chem. 2003, 75, 5413-5421.


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