Environ. Sci. Technol. 2010, 44, 2715–2720
Direct Electricity Recovery from Canna indica by an Air-Cathode Microbial Fuel Cell Inoculated with Rumen Microorganisms GUO-LONG ZANG, GUO-PING SHENG,* ZHONG-HUA TONG, XIAN-WEI LIU, SHAO-XIANG TENG, WEN-WEI LI, AND HAN-QING YU* Department of Chemistry, University of Science & Technology of China, Hefei, 230026 China
Received September 29, 2009. Revised manuscript received February 21, 2010. Accepted March 3, 2010.
Aquatic plants are widely used for phytoremediation, and effective disposal methods should be pursued for their utilization and to avoid further environmental pollution problems. This study demonstrated that, using an air-cathode microbial fuel cell (MFC) inoculated with rumen microorganisms, electricity could be directly produced with a maximum power density of 0.405 W/m3 from Canna indica (canna), a lignocellulosic aquatic plant rich in cellulose, hemicellulose, and lignin, without pretreatment. The mechanisms of the Canna indica degradation in the MFC were elucidated through analyzing the changes of canna structure and intermediates, that is, soluble sugars and volatile fatty acids (VFAs), in the electricity generation process. The results showed that lignin was partially removed and more cellulose became exposed on the sample surface during the electricity generation in the MFC. The electron transfer in this MFC was mainly completed through electron shuttling via self-produced mediators. This work presents an attempt to understand how complex substrates like aquatic plants are decomposed in an MFC during electricity generation. It might, hopefully, provide a promising way to utilize lignocellulosic biomass for energy generation.
electrochemical reactions for energy recovery (6–10). Electricity could be generated from various substrates including cellulose using MFCs (11–13). Lignocellulosic wastes, although insoluble, could be the most abundant, readily available, inexpensive, and reproducible substrate for electricity production. Recent studies have demonstrated that wheat straw and corn stover, after pretreatment, could be partially degraded for electricity generation (14–16). In these works, pretreatment, for example, either neutral or acid steam-exploded hydrolysis, is essential to convert cellulose and hemicellulose in biomass to soluble sugars. Then, the hydrolysates are used for electricity generation. In a recent study, algae was directly converted into electricity in MFCs (17). These previous studies indicate that it is feasible to use other lignocellulosic wastes (e.g., aquatic plants, which are mainly composed of cellulose, hemicellulose, and lignin) for electricity production in MFCs, However, their degrading mechanisms in MFCs remain unclear, and it is critical to understand how complex substrates are decomposed in the electricity generation. Furthermore, to avoid chemical pretreatment of lignocellulosic wastes, it is essential to find out appropriate microorganisms to convert them to soluble sugars and electricity. Our previous studies have demonstrated that the rumens are more efficient in degrading aquatic plants than other anaerobic microorganisms (18, 19). It was recently reported that rumens could be used to inoculate in MFCs to generate electricity from chemical-grade cellulose (20). In their work, MFCs with a two-compartment configuration were employed and ferricyanide was utilized as the oxidant in the cathode. However, it has not been demonstrated whether rumens are able to produce electricity directly from complex lignocellulosic materials (e.g., aquatic plants), rather than pure cellulose. Therefore, in this work an air-cathode MFC inoculated with rumen microorganisms was constructed to generate electricity directly from Canna indica (canna). Canna indica was selected because it has been widely used in phytoremediation (2, 21). The mechanisms of electricity production and canna degradation were explored, and the microbial community in the MFC was also analyzed. This study aimed to demonstrate the feasibility of direct conversion of aquatic plants to electricity by employing rumen microbial communities, and might hopefully provide a new way for recycling lignocellulosic wastes.
Introduction Phytoremediation has been used to remove contaminants such as nitrogen, phosphorus, and heavy metals from polluted water (1). However, in phytoremediation the rapid growth of aquatic plants produces a large amount of biomass, which might in turn become a potential pollution resource if they are not disposed appropriately (1, 2). Aquatic plants can be regarded as a potential renewable resource for energy recovery. Various chemical and biological processes have been proposed to produce ethanol, hydrogen, and methane from lignocellulosic wastes (3–5). Compared with chemical processes, biological processes are more environmentally friendly and less energy intensive. However, information about the biological conversion of aquatic plants into electricity is still sparse. Microbial fuel cell (MFC) is a device that transforms chemical energy stored in organic matters into electricity via * Address correspondence to either author. Fax: +86 551 3601592 (G.-P.Sheng);+865513601592(H.-Q.Yu).E-mail:
[email protected] (G.-P. Sheng);
[email protected] (H.-Q. Yu). 10.1021/es902956e
2010 American Chemical Society
Published on Web 03/12/2010
Materials and Methods Rumen Microorganisms and Canna. The rumen fluid from a goat was stored in a sealed bottle and brought to the laboratory immediately. Pre-enriched microorganisms were inoculated (10%, v/v) in another MFC with canna as substrate. Prior to inoculation, the inoculum solution was filtered through four layer gauze to remove the residual substrates. The anode chamber was autoclaved and flushed vigorously with N2 to remove the oxygen and then filled with 360 mL of the medium and 40 mL of the inoculum. The residual soluble substrates in the inoculum could be neglected. Canna (4 g/L) was added as the sole carbon and energy source. Canna indica samples were collected from a river near our campus in Hefei, China. They were air-dried and then milled to 40-mesh powder, and was then used as the substrate. Chemical analysis of canna shows that hemicellulose, cellulose and lignin accounted for 31, 21, and 9% of total solids, respectively. The crushed canna contained about 3% soluble sugars. The media dosed to the anode contained the following ingredients (per liter): 450 mg K2HPO4, 450 mg VOL. 44, NO. 7, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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KH2PO4, 900 mg NaCl, 300 mg (NH4)2SO4, 120 mg CaCl2 · 2H2O, and 90 mg MgSO4 (19). The conductivity of the solution was 2.55 mS/cm. Air-Cathode MFC Configuration. The configuration of the air-cathode MFC is shown in Supporting Information (SI) Figure S1. The proton exchange membrane (PEM, GEFC10N, GEFC Co., China) and cathode were held at the joint of the tubes. The cathode was Pt-coated carbon paper (2 × 2 cm2, 2 mg cm-2), unless otherwise mentioned, whereas the anode was plain carbon paper (3 × 3 cm2, nonwet-proofed). The surface areas per volume of the anode and cathode electrodes were approximately 2.25 and 1 m2/m3, respectively. The two electrodes had a distance of 6-7 cm. Two ports with an inner diameter of 1 cm were arranged at each reactor chamber for sampling. A magnetic stirrer was used to strengthen mass transfer in the anode solution. The temperature was maintained at 39 ( 1 °C with a temperature controller, and the pH was kept at 6.8-7.0 through automatically dosing 4 mol/L NaOH throughout the experiments. A control test conducted with an anaerobic digester under the same conditions as the canna-fed MFC except no electricity generation. Also, to explore the relationship between canna degradation and electricity generation, two identical MFCs with glucose or acetate as substrate were also operated as a control. Electrochemical Analysis. The output voltage (V) was measured across an external resistor (100 Ω, unless stated otherwise) using a data acquisition system connected to a computer. Current was calculated according to Ohm’s law as I ) V/R, where U is voltage and R is resistance. Power (P) was calculated according to P ) IV. Polarization curve was obtained by varying the external resistance over a range of 10 Ω to 10 kΩ and recording the voltage, the power was then calculated for each resistance as a function of the current. Current density and power density were normalized to the cathode surface area or the MFC volume (400 mL). Internal resistance was derived from the polarization curves (V-I) as the slope estimated with linear regression. The cyclic voltammetry (CV) analysis with the workstation was used to characterize the oxidation-reduction reactions on the electrode surface by measuring the current response at the electrode surface in an unstirred solution. CV was performed in a specific range of potentials at a scan rate of 20 mV/s. The MFC anode, the MFC cathode and an Ag/AgCl electrode served as the working electrode, counter electrode and reference electrode, respectively. The potential was in a range of -600 to 200 mV. All experiments were repeated at least three times. Chemical and Microbial Community Analysis. Soluble sugars were measured using the anthrone-sulfuric acid method (22). Volatile fatty acids (VFAs) were determined with a gas chromatography (GC-6890N, Agilent Inc., U.S.) equipped with a flame ionization detector and a 30 m × 0.25 mm × 0.25 µm fused-silica capillary column (DB-FFAP). Cellulose, hemicellulose, lignin, and ash contents of canna were measured according to Goering and van Soest (23). To analyze the mechanisms of canna degradation by rumens, the X-ray photoelectron spectroscopy (XPS) and X-ray diffraction (XRD) were used to characterize the chemical composition and the surface structure of the raw and degraded canna samples. The denaturing gradient gel electrophoresis (DGGE) method was used to determine the microbial community in the electrode and the solution. The detailed information about the DNA extraction, XPS, XRD, and DGGE analysis could be found in the SI.
Results Electricity Generation in the Canna-Fed MFC. In this cannafed MFC, the output voltage rose rapidly after the substrate dose and maintained at around 0.06 V for 15 h. Then, the 2716
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FIGURE 1. (A) Two cycles of electricity production in the MFC (100 Ω resistor, canna 4 g/L). Arrow indicates the time when the reactor was fed with fresh medium. Inset: the control experiment in the absence of canna; and (B) voltage and power density vs current density. voltage started to decline to a low level and rapidly returned to its original level after 40 h. Later, the voltage increased slightly and reached a maximum value of 0.07 V before a sharp fall at the end of the first cycle (Figure 1A). Similar trends were also observed in the second cycle, while the output voltage was much higher. The total Coulombic recovery of this canna-fed MFC was 400 C/g in the first cycle and increased to 767 C/g in the second cycle. In the control MFC without added canna, the voltage of the MFC was lower than 0.03 V, and dropped to nil quickly after 20 h (Inset of Figure 1A), indicating that the residual metabolite concentration in the inoculum was not of a sufficient level for electricity generation and could be neglected. Figure 1B shows the relationship among voltage, current density, and power density in the MFC. The maximum power density reached 0.405 W/m3 with an open circuit voltage of approximately 0.6 V. The voltage dropped linearly with the increasing current, suggesting that the ohmic losses caused by the resistance between the electrodes and the electrolyte were dominant. From the slope of the linear range of the polarization curve, an internal resistance of 513 Ω was estimated. Cyclic Voltammograms. CV analysis was used to distinguish the electron transfer mechanisms of the electrode reactions involving both direct and indirect electron transfer between the biofilm and the electrode (7). As shown in Figure 2A, no redox couples were detected in the voltammogram obtained with a canna solution of 4 g/L and without rumens. Figure 2B illustrates the CV curve for the electricity generation from the beginning to 80 h in the first cycle, while Figure 2C shows the typical CV curve from 80 h to the test end. When rumens were added, the reduction peaks in the forward scans of the voltammograms were observed at -70 and -144 mV (vs Ag/AgCl), and the oxidation peaks were found at -5 and -85 mV, respectively (Figure 2B). As shown in Figure 2C, the reduction peak in the forward scans of the voltammograms was -160 mV, whereas the additional oxidation peak was -330 mV in the reverse scans. However, at the end of
FIGURE 2. Cyclic voltammetry curves of: (A) a used electrode without rumen inoculated; (B) electrode with rumens from the MFC start-up to 80 h in the first cycle; (C) from 80 h to the end; and (D) at the end of the electricity generation.
FIGURE 3. Profiles of soluble sugars and VFAs in the electricity generating process electricity generation, no oxidation or reduction peaks were observed in either forward or reverse scans (Figure 2D). Production and Consumption of Soluble Sugars and VFAs. Cellulose and hemicellulose in canna could be hydrolyzed to sugars, and further converted to VFAs. Figure 3 shows the concentration profiles of sugars and VFAs during canna degradation and the electricity generation process. A significant amount of sugars and VFAs was produced in the anode chamber. The sugar concentration decreased slightly with the electricity generation at the initial stage. Then, it increased from 151 mg/L at 72 h to 290 mg/L at 191 h. After that, it decreased with the electricity production at a relatively stable level. In the canne fed-MFC, acetate was the predominated VFA species throughout the experiment. After canna was dosed into the MFC, the concentration of VFAs increased to 140 mg/L at 24 h. After that, it decreased rapidly to 59 mg/L at 72 h, and nearly to nil after 191 h (Figure 3). XPS and XRD Results. To elucidate the mechanisms for canna degradation and electricity production, both XPS and XRD were used to evaluate the chemical structure changes of the raw canna and residual canna at the end of test. The evolution of the O/C ratios and relative abundance of C1-C3 in the biodegradation could be used to characterize the changes of canna components. The XPS spectra of C1s of the raw and residual canna samples are, respectively, illustrated in Figure 4, whereas the peak-fitting results and O/C atomic ratios are summarized in Table 1. The results showed that,
FIGURE 4. (A) XPS spectra of C1s of the raw canna; and (B) the residual canna sample at the end of test. after the electricity generation, the relative abundance of C2 and C3 of the canna samples increased remarkably, whereas the relative abundance of C1 decreased by about 18%. The XRD patterns of the raw and residual canna samples in Figure 5 show typical spectra of cellulose materials with the main and secondary peaks at 2θ of 23° and 16°, respectively. The main peak was recognized as an indicator of the presence of highly organized crystalline cellulose, whereas the second and broader peak was attributed to a less organized polysaccharide structure, xylans and other noncellulosic polysaccharides (24). Hemicellulose and lignin in lignocellulose are considered as the amorphous components, while cellulose is regarded to be the crystalline component. As shown in Figure 5, the intensity of the VOL. 44, NO. 7, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. O/C Atomic Ratios and Relative C1-C3 Peak Areas of Canna and Its Main Components relative area (%) material
O/C
C1
C2
C3
theoretical values
lignin cellulose hemicellulose wax
0.33 0.83 0.80 0.04-0.11
49 0 0 94-100
49 83 83 0
2 17 17 0-6
measured values
raw canna residual canna
0.24 0.41
76.5 58.0
14.9 29.3
8.6 12.7
Discussion
FIGURE 5. X-ray diffraction patterns of: (A) raw canna; and (B) the residual canna sample at the end of test. amorphous region of the residual canna was lower than that of the raw canna, whereas its intensity of the crystalline region was greater than that of the raw canna. This implies the disruption of the crystal structure of canna and an increase in the relative content of cellulose after canna was subjected to the rumen degradation and electricity generation. Microbial Community Changes. The DGGE profiles in SI Figure S2 show the changes in microbial community composition of the inoculum rumen fluid, suspended and anode-attached cultures after its utilization for canna degradation and electricity generation in the MFC. Different main bands were noticed in each sample, whereas some common bands were present in all cases. Bands 1, 2, 4, and 5 were extremely enriched and preferably showed up in the anode-attached sample, compared to the initial inoculums and the suspended cultures. Band 3 was observed only in the anode-attached community. Bands 6-9 were dominant in the inoculum rumen fluid, but their intensity decreased after the electricity generation. The bands that appeared visually to be either lost or gained were excised from the DGGE gel for sequencing analysis. DNA sequences were compared to the GenBank database using BLASTn search (see SI Table S1). Bands 2 and 3 had a high similarity to Acinetobacter sp. (99%). Bands 4-6 showed the highest identity (100%) to Trichococcus pasteurii, Bacteroides sp. and Uncultured Bacteroidetes bacterium, respectively. Bands 1, 7, 8, and 9 were closely related to unclassified environmental samples. 2718
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Our previous study has shown that rumen microorganisms could degrade aquatic plants effectively (18), whereas the present work further demonstrates that it is feasible to directly convert aquatic plants to electricity in an air-cathode MFC via the microbial catalysis of rumens. It is a new and promising way to couple lignocellulosic biomass disposal with energy recovery. The maximum power production of this cannafed MFC inoculated with rumen microorganisms reached 405 mW/m2. Connection between Electricity Generation and Canna Degradation. VFAs and sugars were the two main intermediates in canna degradation. From the profiles of the electricity generation and the intermediate products, the canna degradation in the MFC could be divided into two stages. In the first stage, the output voltage increased rapidly after the substrate dose, and after a short time it declined to its original level (Figure 1A). Simultaneously, the concentration of VFAs increased, while the concentration of soluble sugars decreased slightly (Figure 3). As the hydrolysis phase is the rate-limiting step of anaerobic degradation of ligonocellulosic wastes (18), the VFAs produced at the initial stage and electricity generation might be mainly originated from the soluble sugars in canna. After the first stage, the voltage increased slightly and decreased sharply at the end of cycle. At the same time, the concentration of VFAs dropped rapidly to nil, while the sugar concentration slightly increased and then decreased. This implied that the electricity production at this stage was mainly attributed to the hydrolytic and acidogenic products of canna. The anaerobic conversion process of lignocellulosic biomass by rumens usually involves three sequencing steps, that is, hydrolysis, acidification and methanogenesis. In a control test conducted with an anaerobic digester under the same conditions as the canna-fed MFC except no electricity generation, acetate, and propionate were the major aqueous fermentative products, while butyrate, i-butyrate and valerate were also formed in smaller quantities. The biogas produced in the control reactor was composed of carbon dioxide, methane, and little hydrogen. In the MFCs with rumens as a biocatalyst, the canna conversion pathway was somewhat different. In the canna-fed MFC, the soluble sugars were produced from lignocellulose hydrolysis, and then converted to VFAs, among which acetate was the main species. An increase in sugar content was observed when lignocellulose hydrolysis occurred, but the VFAs were of a low level at this stage, as they were converted to electricity; At the end of canna degradation, the VFA concentration was almost nil. In the control tests with glucose or acetate as substrate for MFCs, it was also found the sugar content declined rapidly when glucose was used as the substrate, and the VFA content increased initially, but then decreased. On the contrary, the acetate content kept declining when it was used as the substrate for the MFC. These results implied that the canna in the MFC was initially hydrolyzed to soluble sugars, which were
TABLE 2. Summary of Cellulose, Hemicellulose, And Lignin Fractions in Raw and Residual Canna Samples and Their Removal Efficiencies in the MFC fractions (%)
cellulose hemicellulose lignin
raw canna
residual canna
21 ( 3 31 ( 2 9(1
24 ( 2 26 ( 3 15 ( 4
removal efficiencies (%) 46 ( 7 61 ( 8 22 ( 8
then converted to VFAs. The electricity was produced in the acidification and VFA utilization processes. To reconfirm the observations above, the contents of cellulose, hemicellulose and lignin in both raw and the residual canna samples were measured. Approximately 46% of cellulose, 61% of hemicellulose, and 22% of lignin were degraded in this rumen-inoculated MFC, as shown in Table 2. The macromolecular properties and structural characteristics of lignin make its biodegradation difficult (25), but notable lignin degradation efficiency was achieved in this MFC, suggesting that lignin could be degraded or become soluble by the rumen microorganisms and then be converted to electricity. This result further confirms that rumen microorganisms could be utilized for bioconversion of lignocellulosic wastes into electricity. Change of Canna Structure in Electricity Generation. The surface characteristics of canna are related to the variation of the molecular structure and the corresponding local element distribution (18). The decrease in C1 and the increase in C2 and C3 also indicate either a decrease in the lignin content or an increase in the cellulose or hemicellulose content in canna samples. The substantial increase in O/C atomic ratios suggests that wax and lignin on the canna surface were partially degraded or converted to electricity by rumens, and that the residual canna was rich in cellulose or hemicellulose, compared with the raw canna. This result was in agreement with those of chemical composition and XRD analysis of the raw and residual canna samples. The possible reason was that the degradation efficiencies of lignin, hemicellulose and cellulose by rumens were different, resulting in an increase in relative fraction of cellulose in canna when it was used for electricity generation in the MFC. Electron Transfer Mechanisms in the Rumen-Inoculated MFC. CV has been used as a standard means to characterize electron transfer mechanisms between the culture and anodes in an MFC (26). There were no redox peaks in these CV curves (Figure 2A), indicating that there were no redox components in the substrate. When the MFC was inoculated with rumen fluid in the absence of canna, there were no redox peaks either. This demonstrated the pre-enriched inoculum had no mediators. However, when both rumens fluid and canna were added into the MFC, the reduction and the oxidation peaks in the forward scans of the voltammograms were observed (Figure 2B). At the end of electricity generation, no oxidation or reduction peaks were observed in either forward or reverse scans (Figure 2D). After redose of canna to the MFC, the redox peaks emerged again. Therefore, these peaks demonstrated that the electron transfer in this MFC was mainly through electron shutters, which were produced in the canna degradation. At different stages of electricity generation, the redox peak locations of the mediators were different (Figure 3B and C). This also suggested that the mediators were produced by the rumens in the canna degradation. Significance of This Work. This work confirms that direct electricity production from aquatic plants by rumens could be coupled effectively with the disposal and recycling of lignocellulosic wastes. Although the energy recovery ef-
ficiency of the present system is not high, it shows a promising way for the further utilization of aquatic plants for energy recovery. Considering that a huge amount of aquatic plants is produced from phytoremediation in China and other countries, the potential power generation from their utilization in MFCs would be substantial. In addition to aquatic plants, other types of lignocellulosic wastes could also be used for electricity generation in such a MFC system. To make the direct electricity generation from lignocellulosic wastes in the MFC competitive with other technologies, for example, ethanol production and anaerobic digestion in combination with combustion, further studies should be conducted to find out more efficient ways to improve the energy recovery efficiency and power density from aquatic plants in MFCs. The electricity generation capacity of our system is still limited by many factors, such as relatively simple reactor configuration, the large electrode spacing and the low canna hydrolysis rate. Thus, approaches should be explored to resolve these problems. For instance, for the reactor architecture design, in addition to the solid-liquid mass transfer between the electrode and soluble organics, the solid-solid mass transfer between the electrode and solid particulate should also be taken into account. These warrant further investigation.
Acknowledgments We thank the CAS (KZCX2-YW-QN504; KJCX2-YW-H21-01), and the NSFC (50625825 and 50878203) for the partial support of this study.
Supporting Information Available Additional information including two figures and one table. This material is available free of charge via the Internet at http://pubs.acs.org.
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ES902956E
