Solar-Driven Microbial Photoelectrochemical Cells with a Nanowire

Oct 12, 2010 - We report a self-biased, solar-driven microbial photoelectrochemical cell (solar MPC) that can produce sustainable energy through coupl...
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Solar-Driven Microbial Photoelectrochemical Cells with a Nanowire Photocathode Fang Qian,* Gongming Wang, and Yat Li* Department of Chemistry and Biochemistry, University of California, Santa Cruz, California 95064, United States ABSTRACT We report a self-biased, solar-driven microbial photoelectrochemical cell (solar MPC) that can produce sustainable energy through coupling the microbial catalysis of biodegradable organic matter with solar energy conversion. The solar MPC consists of a p-type cuprous oxide nanowire-arrayed photocathode and an electricigen (Shewanella oneidensis MR-1)-colonizing anode, which can harvest solar energy and bioenergy, respectively. The photocathode and bioanode are interfaced by matching the redox potentials of bacterial cells and the electronic bands of semiconductor nanowires. We successfully demonstrated substantial current generation of 200 µA from the MPC device based on the synergistic effect of the bioanode (projected area of 20 cm2) and photocathode (projected area of 4 cm2) at zero bias under white light illumination of 20 mW/cm2. We identified the transition of rate-limiting step from the photocathode to the bioanode with increasing light intensities. The solar MPC showed self-sustained operation for more than 50 h in batch-fed mode under continuous light illumination. The ability to tune the synergistic effect between microbial cells and semiconductor nanowire systems could open up new opportunities for microbial/nanoelectronic hybrid devices with unique applications in energy conversion, environmental protection, and biomedical research. KEYWORDS Microbial photoelectrochemical cells, Semiconductor nanowires, Shewanella oneidensis MR-1

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nergy crisis and environmental pollution are projected as the major global problems in the 21st century. Development of new energy solutions with minimum impact on the environment is critical to the continuation of economy growth and to maintain a green fit of inhabitation for human beings. In this regard, microbial fuel cells (MFCs) hold great promises to address both issues simultaneously, by producing electricity from microbial conversion of biodegradable organic matter.1-3 The essential of MFC technology is the usage of a unique type of electrogenic bacterial strains, which can bio-oxidize organic matter to produce electrons in their central metabolism and transfer part of these electrons extracellularly to an external electrode. Previous reports have suggested extracellular electron transfer via various pathways, including direct membrane protein/anode coupling,4,5 through conductive pili,6-8 and/or self-secreted electron shutters9,10 (Figure S1, Supporting Information). In a MFC device, these bacteriagenerated electrons flow through an external circuit to the cathode, where they are used to reduce oxidants in the catholyte, such as oxygen and metal complexes. If protons serve as the sole electron acceptor in catholyte, hydrogen gas would be generated at the cathode (Figure S1, Supporting Information), and this type of MFC is called microbial electrolysis cell (MEC).11 In comparison to water electrolysis for hydrogen generation, MECs oxidize organic matter that typically has lower oxidation potential than water, therefore requiring a lower energy input and without the need of

expensive anodic catalysts. MEC processes can achieve the substrate-to-hydrogen conversion efficiencies of 72-93%.12 While MEC represents an environmental friendly approach for hydrogen generation, thermodynamic analysis predicts that the microbial electrohydrogenesis process requires additional energy input to overcome the energy barrier in converting organic matter to hydrogen. This energy is typically supplied in terms of an external bias of a theoretical minimum of 0.11 V while practically at least 0.2 to 1 V due to electrode overpotential and the device resistance.11,13,14 The need of external bias reduces the overall energy recovery ratio and makes MEC less attractive. Considerable efforts have been made on optimization of MEC reactors,12,15 design of anodes,16-18 and catalysts19 to reduce the above-mentioned energy losses. Alternatively, to obtain the required energy from a renewable energy source is a promising approach that can fundamentally address the issue. Solar-assisted MEC has recently been reported, where an external solar cell is incorporated with the MEC device to provide the required energy.20 However, the coupling of solar cell and MEC does not change the operation fundamentals of MEC and would increase the material and device fabrication cost. To date, self-sustained, efficient, and costeffective microbial electrohydrogenesis still represents significant challenges at both the conceptual and device levels. To realize a solar-driven MFC/MEC, the key challenge is the integration of solar light conversion with microbial electricity generation. Here we report a new self-biased, solar-driven microbial photoelectrochemical cell (solar MPC) that addresses this challenge by coupling an electricigencolonizing anode with a semiconductor nanowire-arrayed cathode. As shown in Figure 1a, the solar MPC device was

* To whom correspondence should be addressed. E-mail: (F.Q.) [email protected]; (Y.L.) [email protected]. Received for review: 08/23/2010 Published on Web: 10/12/2010 © 2010 American Chemical Society

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values of -0.32 to -0.24 V for OmcA and ∼ -0.1 V for MtrC versus normal hydrogen electrode (NHE).10,22 To reduce protons at the cathode, the semiconductor must be p-type and has a conduction band edge more negative than the H+/ H2 potential at neutral pH (-0.41 V).11 In the dark, the Fermi level of p-type semiconductor at equilibrium typically lies below the H+/H2 potential, and thus proton reduction is thermodynamically unfavorable. The bioelectrons generated at anode also cannot travel to the cathode without electron acceptors. Upon light illumination, photogenerated electrons at semiconductor conduction band can reduce protons in the catholyte, while the holes in valence band recombine with the biological electrons generated at anode. In this manner, the inorganic photocathode and the bioanode function synergistically to combine the energy from solar light and organic substrate for driving microbial electricity generation. In this work, we used Cu2O nanowires as photocathode to demonstrate the concept of solar-MPC, due to its favorable band structures (-0.69 V for CB and 1.51 V for VB vs NHE at pH 7.0)23 for coupling microbial electron transfer and proton reduction aforementioned. Unintentionally doped Cu2O is a p-type semiconductor due to the existence of oxygen vacancies.24 It is an environmentally benign material with optimal bandgap of 2.2 eV for visible light absorption. Additionally, nanowire structures offer distinct advantages compared to bulk materials, including large surface-area for proton reduction and short electron diffusion length, which could enhance the carrier separation and collection efficiency at the cathode.25 The Cu2O nanowire photocathode was synthesized by a simple and scalable wet chemical method reported elsewhere.26,27 We first prepared Cu(OH)2 nanowires via surface oxidation of a copper coil in a NaOH solution with (NH4)2S2O8 as oxidizing agent, followed by thermal treatment at 450 °C in air for 1 h to convert Cu(OH)2 to Cu2O nanowires (Experimental Method, Supporting Information). Scanning electron microscope (SEM) images showed that the surface of the copper foil was covered by dense nanowires with uniform morphologies (Figure 2a). The nanowires have an average diameter of 300-400 nm and length of 5-10 µm. Powder X-ray diffraction (PXRD) spectra were collected from the nanowires before and after thermal annealing. PXRD data revealed the successful growth of Cu(OH)2 nanowires on copper foil based on its characteristic diffraction peaks26 (Figure S2, Supporting Information). After thermal oxidation, the diffraction peaks of Cu(OH)2 disappeared, and the new diffraction peaks were indexed to Cu2O cubic and CuO monoclinic structures, respectively (Figure S2, Supporting Information). On the basis of the peak intensity, we confirmed that most Cu(OH)2 nanowires have been converted into Cu2O nanowires with a small fraction of CuO nanowires. To evaluate the performance of Cu2O nanowires as photocathode, we conducted photoelectrochemical (PEC) measurements of Cu2O nanowire-arrayed cathode in a three-

FIGURE 1. General working mechanism of a solar MPC. (a) Schematic diagram of a dual-chamber MPC. The cathode and the anode chamber were separated by a CEM. (b) Corresponding energy diagram illustrates the carrier generation and charge transfer at the virtual interface between microbial and semiconductor systems. CB, VB, and EF are respective initials for conduction band, valence band, and Fermi level. Solid and empty red dots represent photogenerated electrons and holes. Black dots represent electrons generated from bacterial cells.

configured as a dual-chamber electrochemical cell where the cathode and the anode chamber were separated by a cation exchange membrane (CEM). A p-type Cu2O nanowire-arrayed photocathode was immersed in an anoxic buffered solution for proton reduction, and a carbon anode preinoculated with electrogenic bacterial strain, S. oneidensis MR-1, was used to generate electrons from organic substrate. The electrodes were connected through an external circuit. Note the energy band-bending at the semiconductor/electrolyte interface will facilitate the efficient charge separation21 (Figure 1b), and the solar MPC virtually interface bacterial cells and photocathode without physical contact, allowing a wide range of semiconductors coupled with microbial electricity generation, even those reported with microbial toxicity. Central to the success of solar MPCs is the rational selection of semiconductor materials that can interact electrically with electricigen strains. The coupling of the photocathode with microbial electrohydrolysis is determined by the semiconductor band edge positions relative to the redox potential presented by bacterial cells (Figure 1b). To receive microbial electrons, the semiconductor should have a valence band edge more positive than the electrochemical potentials of bacterial outer membrane c-type cytochrome (Omc) proteins. For instance, Shewanella cells have reported © 2010 American Chemical Society

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to pH 7.0. Figure 2b shows the linear sweep voltammagrams recorded from a representative nanowire photocathode in the dark and with white light illumination (Xenon lamp coupled with A.M. 1.5 filter). While the dark scan from -0.05 to -0.4 V vs Ag/AgCl led to a small current density in the range of 10-2 mA/cm2, the PEC showed photocurrent densities up to 0.3 and 0.7 mA/cm2 at a bias of -0.4 V vs Ag/ AgCl under the light power densities of 50 and 100 mW/cm2, respectively. The pronounced photocurrent suggested efficient photon absorption and charge separation at the semiconductor/catholyte interface. The Mott-Schottky plot of the Cu2O nanowire cathode showed a negative slope (Figure 2b, inset), confirming the nanowires were p-type material with hole conduction. Amperometric I-t curve collected at a bias of -0.3 V vs Ag/AgCl with light on/off cycles showed that the cathode have reproducible photocurrent generation in response to light illumination of 100 mW/cm2 (Figure 2c). The spike observed in each light on/ off cycle was due to the transient effect in power excitation, and the photocurrent returned to a steady level in several seconds. Taken together, the PEC data demonstrated that the p-type Cu2O nanowires can serve as an excellent photocathode with rapid photoresponse and pronounced photocurrent generation. The bioanode, where the biomass-to-electricity conversion takes place, plays an essential role in the solar-MPCs. Electrochemically active bioanodes were prepared in a conventional MFC using a previously reported method with only exception of adopting a 30 mL dual-chamber MFC reactor (Experimental Method, Supporting Information).28,29 Carbon cloth was used as electrode materials in which bacterial cells gradually formed a biofilm covering the anode surface. Using trypticase soy broth (TSB) as growth medium, ferricyanide buffer as catholyte and an external resistor of 1-10 kΩ, these MFCs generated peak current densities in the range of 5-30 µA/cm2 depending on specific reactor configuration.29 The typical current versus time plot obtained of such a MFC was shown in Figure S3, Supporting Information. In each feeding cycle, the peak current densities were about 15 µA/cm2, sustained for ca. 24 h, and generated an average charge density of 7.2 mC/cm2. The observed reproducible current generation in response to substrate addition suggested successful preparation of a bioanode. The SEM image of the bioanode (Figure 3a) revealed apparent bacterial cell growth on the carbon cloth fibers. The cells were rod-shaped with typical length of 2-3 µm, consistent with the morphologies of S. oneidensis cells. High-density cell segregates thrived in the gaps between the carbon fibers, and individual cells were more frequently seen attached on the exposed fiber surface. To evaluate the electrochemical activity of as-prepared bioanodes, we measured the cyclic voltammetry (CV) of the bioanode in a three-electrode electrochemical cell. A comparative experiment with bare carbon cloth anode of the same projected area in TSB medium was also carried out as

FIGURE 2. Cu2O nanowire-arrayed photocathode. (a) SEM image of Cu2O nanowires grown on a copper foil, scale bar is 20 µm; inset: magnified SEM image of Cu2O nanowires, scale bar is 5 µm. (b) Linear sweep voltammagrams, collected from Cu2O nanowires at a scan rate of 10 mV/s at applied potentials from -0.05 to -0.4 V vs Ag/AgCl in the dark (black line), at 50 (blue line), and 100 mW/cm2 (red line). Inset: Mott-Schottky plot of Cu2O nanowires collected in the dark at frequency of 1 kHz. Dashed lines represent the extrapolated lines from the linear portion of the Mott-Schottky plot. (c) Amperometric I-t curves recorded from Cu2O nanowire cathode at a bias of -0.3 V vs Ag/AgCl with light on/off cycles at light intensity of 100 mW/cm2.

electrode cell with a Pt wire as a counter electrode and an Ag/AgCl reference, in a 0.5 M Na2SO4 aqueous solution buffer © 2010 American Chemical Society

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tential change of the bioanode and the photocathode was measured under open circuit condition (Figure 4a). Under a light illumination intensity of 100 mW/cm2 (A.M. 1.5), the p-Cu2O nanowire photocathode exhibited instant photoresponse with a photovoltage of about 0.25 V versus Ag/AgCl. The bioanode yielded a constant potential at about -0.3 V versus Ag/AgCl at the same condition without photoresponse. The open circuit voltages of MPCs we studied under illumination were in the range of 0.4-0.6 V, comparable to the value reported for ferricyanide-driven MFCs.29,31 To investigate the performance of solar MPCs, we collected I-t plots from three devices at zero bias and a light illumination of 20 mW/cm2 (Figure 4b), including (1) a solar MPC composed of a bioanode and a p-Cu2O nanowire photocathode (red); (2) a MEC using the same bioanode but a Pt cathode (blue); and (3) a PEC device using the same p-Cu2O nanowire photocathode but a Pt anode (green). In absence of external bias, the PEC device with nanowire cathode showed a negligible photocurrent of ∼0.6 µA under the light. It confirmed that the PEC device cannot be operated at zero bias. Meanwhile, the MEC device displayed a small background current of ∼20 µA (∼1 µA/cm2) due to the potential difference between cathode and anode, which were commonly observed in MFC devices.28,32 Without a semiconductor cathode, the MEC did not respond to light irradiation, as expected. These data confirmed no current generation at zero bias when the device contained a photocathode or bioanode alone. In contrast, the MPC device showed a substantial net current gain of ∼200 µA (50 µA/ cm2) under light illumination of 20 mW/cm2 at zero bias. The background current of ∼100 µA (∼25 µA/cm2) in MPC was comparable to that in a Cu2O nanowire PEC device at -0.3 V vs Ag/AgCl in the dark (∼30 µA/cm2) (Figure 2b) and thus was attributed to the negative bias imposed by the bioanode (Figure 4a). The results unambiguously declare the successful demonstration of self-biased, solar-driven MPC based on the synergistic effect of nanowire photocathode and bioanode. Furthermore, the MPC efficiency is expected to be determined by the performance of both bioanode and photocathode, as well as their electrical interaction. To identify the rate-limiting step of MPC operation, we measured the current generation of the solar MPC as a function of light intensity. As shown in Figure 4c, the current generation from a representative solar MPC (red) at zero bias increased drastically with light intensity until 10 mW/cm2 and then increased slowly afterward, indicating that the current generation in MPC was saturated under intense light irradiation. In contrast, the current from the PEC using the same photocathode (green) biased at -0.1 V vs Ag/AgCl did not approach saturation until ca. 150 mW/cm2. This comparison suggested that the solar MPC worked mostly in the anodelimiting region. In this region, the number of electrons transferred from microbial cells is less than the number of photogenerated holes at cathode. The excess holes will recombine with photogenerated electrons and thus limit the

FIGURE 3. Preparation and electrochemical studies of bioanodes. (a) SEM image of a Shewanella-colonizing carbon cloth anode. Scale bar is 5 µm. (b) Cyclic voltammograms collected at a scan rate of 10 mV/s from a live bioanode (blue) and a bare carbon cloth electrode (red) in the same TSB medium.

a control. As shown in Figure 3b, while there were no redox peaks observed from the bare carbon electrode in all the potential regions studied (red curve), the CV collected from the live bioanode (blue curve) clearly showed a well-defined redox couple with distinct cathodic peak at -0.47 V and anodic peak at -0.41 V versus Ag/AgCl, respectively. The potentials of the redox couple were consistent with previous reported values of Omc proteins (-0.32 to -0.24 V for OmcA and ∼-0.1 V for MtrC vs NHE),10,22 suggesting the observed electrochemical activity of the bioanode originated from the c-type cytochrome systems of Shewanella. Significantly, the current density in the CV obtained from the live bioanode was substantially higher than that from the bare carbon anode in TSB, indicating bacterial cells mediated electron transfer from carbon sources to the anode.30 To validate the solar MPC concept, we assembled a nanowire photocathode (projected area of 4 cm2) and a live bioanode (projected area of 20 cm2) in a dual-chamber photoelectrochemical cell. TSB medium and potassium phosphate buffer solution (100 mM, pH 7.0) were used as anolyte and catholyte, respectively. The photoinduced po© 2010 American Chemical Society

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FIGURE 5. Current vs time plot of the solar MPC operated in a batchfed mode at zero bias under the light illumination of 20 mW/cm2, showing sustainable current generation in response to substrate addition.

cathodic reduction reaction. The insufficient electron generation at the bioanode could be attributed to the slow electron transfer dynamics at the bacterial cell/anode interface;33 therefore, the photocathode was not working to its full capacity for proton reduction. We observed similar current versus light intensity profile for all devices that we studied (data not shown), although the absolute current values could differ in different devices due to expected variation of parameters in individual MPCs (e.g., internal resistance, bioanode activity, etc.). Increasing the anode-tocathode area ratio and/or improving the bacterial cell/anode electron transfer activity should help tune the relative capacities of the electrodes and subsequently enable a larger current generation at a more intense light irradiation. Last, we measured the sustainability of a solar MPC working in the self-biased manner, using a 1 mL flat-panel MFC with cathode and anode area of both 4 cm2. The device was operated in batch-fed mode at zero bias under continuous light illumination of 20 mW/cm2, and the current generation of the MPC was recorded as a function of time. As shown in Figure 5, we observed continuous current generation from the MPC in two consecutive feeding cycles on TSB and lasting for more than 50 h. The current decreasing to the baseline indicated the depletion of nutrient and toxic metabolite build-up, and the replenishment of fresh TSB medium led to a steady current restoration to a peak value of 25-35 µA. The relatively small photocurrent was expected due to the high internal resistance of the miniature devices. Note the I-t curve of a batch-fed MPC was consistent with that of a conventional ferricyanide-driven MFC device,28 yet the MPC was driven by light-induced cathodic reaction. The sustainability measurement declares that the solar-driven MPC can be operated at a long-time scale and continuously operable if there is a continuous supply of organic substrate and solar illumination.

FIGURE 4. Characterization of solar MPC devices. (a) Light-induced potential change of a Cu2O nanowire photocathode (green) and a bioanode (blue) at open circuit conditions. (b) I-t curves recorded from (i) a Cu2O nanowire-based solar MPC with a live bioanode (red); (ii) a MEC with the same bioanode and a Pt cathode (blue); and (iii) a PEC with the same Cu2O nanowire photocathode and a Pt anode (green). All the measurements were collected at zero bias under light illumination of 20 mW/cm2 using two electrode configuration. (c) Current vs incident light intensity plots of a solar MPC (red) collected at zero bias and a PEC using the same photocathode (green) collected at -0.1 V vs Ag/AgCl. © 2010 American Chemical Society

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In summary, we have developed a solar-driven, selfbiased MPC that coupled a bacterial-colonizing bioanode with a semiconductor nanowire cathode in utilizing solar energy for microbial electricity generation. The working mechanism of extracellular electron transfer at the virtual microbial/semiconductor interface was described, and the criteria of semiconductor cathode for driving a solar MPC were discussed. Employing a p-type Cu2O nanowire-arrayed photocathode and Shewanella oneidensis MR-1 as anodic inocula, we have demonstrated efficient current generation in this hybrid system at zero bias. The present studies will provide new insight into the biological energy research including light-assisted biological hydrogen production, and more importantly, open up exciting opportunities at the unique interface between semiconductor nanowires and bacterial systems.

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Acknowledgment. We are thankful for the helpful discussion with Zhen He. We thank Professor Jin Z. Zhang for offering PEC measurement facilities. Y.L. and F.Q. acknowledge the support of this work by NSF (CBET 1034222) and faculty research funds granted by the University of California, Santa Cruz.

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Supporting Information Available. Experimental methods, PXRD, and MFC data. This material is available free of charge via the Internet at http://pubs.acs.org.

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DOI: 10.1021/nl102977n | Nano Lett. 2010, 10, 4686-–4691