Environmental Pollution 158 (2010) 185191

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Environmental Pollution
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Alteration of sediment organic matter in sediment microbial fuel cells

Seok Won Hong a, Han S. Kim b, Tai Hak Chung c, *
a

Center for Environmental Technology Research, Korea Institute of Science and Technology, P.O. Box 131, Cheongryang, Seoul 130-650, Republic of Korea Environmental Engineering, Advanced Technology Fusion, Konkuk University, 1 Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of Korea c Department of Civil and Environmental Engineering, Seoul National University, 599 Gwanak-ro, Gwanak-gu, Seoul 151-742, Republic of Korea
b

Sediment microbial fuel cells can stimulate the humication of sediment organic matter.

a r t i c l e i n f o
Article history: Received 1 May 2009 Received in revised form 12 July 2009 Accepted 17 July 2009 Keywords: Microbial fuel cell Electricity generation Sediment organic matter Anaerobic oxidation Humication

a b s t r a c t
The alteration of physico-chemical properties of sediment organic matter (SOM) incubated under current-harvesting conditions as well as no-current producing conditions over 120 days using sediment microbial fuel cell systems was examined. The SOM was microbially oxidized under anaerobic conditions with an electrode serving as a terminal electron acceptor. It was found that SOM around the electrochemically-active electrodes became more humied, aromatic, and polydispersed, and had a higher average molecular weight, along with its partial degradation and electricity generation compared to that for the original sediment. These changes in SOM properties were analogous to those commonly observed in the early stages of the SOM diagenetic process (i.e. humication). Such a humication-like process was evidently more stimulated when electrical current was produced than no-current condition. These new ndings associated with microbially-catalyzed electricity generation may present a potential for the energy-efcient remediation, monitoring, and/or management of the geo-environment. 2009 Elsevier Ltd. All rights reserved.

1. Introduction Organic matter is known as a derivative of plant and animal detritus, fecal matter, dead bacteria and plankton, and even anthropogenic organic materials in soils and sediments comprising subsurface systems (Kruge et al., 1998). Soil and sediment organic matter (SOM) is a highly complex and heterogeneous composite initially resulting from the physical, chemical, and microbial evolution of biopolymeric materials. These biopolymers are further decomposed to fulvic and humic acids, kerogen, and even black carbonaceous materials under various degrees of diagenetic processes (Huang and Weber, 1997). Since SOM is believed to serve as a principal geo-sorbent for hydrophobic organic contaminants (HOCs) in soils and sediments (Huang and Weber, 1997; Xing, 2001), signicant attention has been given to its inuence on the mobility, reactivity, bioavailability, and ultimate fate of HOCs in geo-environments. In this regards, the association of HOCs with SOM has been assessed by analyzing various physico-chemical properties of SOM with regard to its geological evolution processes (i.e. diagenesis) in a large number of studies (Huang and Weber, 1997; Grathwohl, 1990). Hence, SOM characterization has been noted as a vital effort for the understanding and evaluation of the

* Corresponding author. Tel.: 82 2 880 7369; fax: 82 2 889 0032. E-mail address: thchung@snu.ac.kr (T.H. Chung). 0269-7491/$ see front matter 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2009.07.022

behavior and fate of HOCs in contaminated subsurface systems and for successful remediation actions. Geo-microbial reactions play an important role in environmental determinants under natural conditions, in particular, during the early stages of SOM diagenetic processes (i.e. humication, Stevenson, 1982; Aiken et al., 1985). It has been also known that the characteristics of SOM can be altered on account of microbial metabolic processes based on different types of nal electron acceptors (e.g., aerobic, anoxic, and obligate anaerobic conditions). Only a limited number of studies, however, have addressed microbial impacts on the physico-chemical properties of SOM and its binding characteristics with HOCs. Coates et al. (2000) reported that the microbial reduction of humic acids can result in their different associations with inorganic and organic contaminants because of changes in their electronegativities. Kim and Pfaender (2005) have also demonstrated that the physico-chemical properties of SOM became substantially different under various redox conditions, which stimulated the humication of SOM and subsequent favorable bindings with pyrene. Microbial fuel cell (MFC) systems have recently been of great interest as a potential candidate for future alternative energy production. Organic substances are converted into electricity via the action of bacteria as catalysts in MFCs (Chaudhuri and Lovley, 2003). A typical MFC system consists of two electrodes: an anode for fuel oxidation and a cathode for oxygen reduction, and they are commonly separated by a proton-conducting membrane. Under

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S.W. Hong et al. / Environmental Pollution 158 (2010) 185191 Following the rainy season in summer this stream often becomes moderately eutrophic or hypereutrophic. The sampling was performed using a Ponar type grab sampler (2.4-L vol.). All samples including surface water were placed into clean polycarbonate jars (Nalgene, Fisher Scientic) with no headspace gas (i.e. air) and transported to the laboratory in a cooler box with ice packs. All sediments were passed through a 2-mm sieve to remove plant debris, macrofauna, and other large terrestrial leaves and then homogenized by mixing with a stainless steel spatula prior to use. Physical characteristics of the sediment are provided in Table 1. 2.2. Sediment MFCs All sediment MFCs were made of plexiglass. Aliquots of 50-g wet sediment and 120-mL stream water were loaded into the lower and upper part of each sediment MFC, respectively. Over the course of reactor run, water loss due to evaporation was compensated daily by adding distilled water. The electrodes used in this experiment were graphite felt (GF series, Electrosynthesis, Amherst, NY, USA). The dimension of the anode was 150 45 3 mm (length width thickness). To minimize mass transfer limitation within the sediment as well as to increase the opportunities for contact between sediment and anode, each anode was placed along an acrylic holder as described in Fig. 1. The cathode (40 35 3 mm) was bare graphite felt and placed parallel to the anode and 4 cm above the sedimentwater interface. Air was introduced by a ne bubble diffuser suspended in the overlying water in order to maintain oxic conditions (dissolved oxygen levels ranging from 3 to 4 mg O2 L1). Both anode and cathode were connected by a platinum wire and an insulated copper wire to an external load. All sediment MFCs were kept in a dark chamber at 20 0.5  C and the external circuit resistance was xed at 10 U under closed-circuit conditions. Four closed-circuit sediment MFCs were operated in parallel and each was sacriced at each sediment collection time. A sediment MFC was also operated under open-circuit conditions (i.e. innite external resistance). The voltage difference between two electrodes across a load was measured using a digital multimeter (Model 2700, Keithley Instruments, Cleveland, OH, USA). Data were recorded hourly on a spreadsheet using ExceLINX (Keithley) via an interface card (GPIB Interface Boards, Keithley) linked to a personal computer. The recorded voltage was converted into current using Ohms law (current voltage/resistance). Current density was also calculated by dividing the current by the apparent surface area of anode. 2.3. SOM fractionation The sediments incubated under closed-circuit conditions were collected at 30, 60, 90, and 120 days of incubation while the sediment incubated under open-circuit conditions was sampled after 120 days. The surface sediment samples (1 cm down from the sedimentwater interface) exposed to aerobic conditions were discarded from the closed- and open-circuit sediment MFCs. The remainder samples collected from the sediment MFCs, including the original sediment (hereafter referred to as control), were air-dried and ground. The chemical fractionation of sediments based on differences in solubility in alkaline and acid solutions was performed according to the procedure recommended by the International Humic Substances Society (Senesi and Loffredo, 1999) with a slight modication. In this study, the fractionated SOM samples were classied into three factions as follows: biopolymer (BP), fulvic acid (FA), and humic acid (HA). Detailed procedures for the SOM extraction and fractionation are provided in the Supplementary section. The organic carbon content of each SOM fraction was quantied as total organic carbon (TOC) concentration. 2.4. Analytical procedures Redox potentials (Eh) were measured using a combined Pt and Ag/AgCl electrode (9678 BNWP, Thermo Orion, Beverly, MA, USA). The probe was directly inserted into the sediment after disconnecting the circuit and the Eh values obtained after an equilibration period of 1 h were corrected based on the standard hydrogen electrode (SHE). Conductivity was also measured using a 105 A plus conductivity meter (Thermo Orion). Elemental analysis was performed using an EA 1110 analyzer (CE Instruments, Milan, Italy) to determine the atomic ratios of C, H, N, and S of organic matter extracted from the sediment. Ash content was determined by combusting the extracted organic matter in a mufe furnace at 800  C for 3 h. Oxygen content was determined by difference as described elsewhere (Loffredo et al., 1999). Organic carbon concentrations in the aqueous samples were determined by a TOC analyzer (TOC-V CPH, Shimadzu, Kyoto, Japan). Spectroscopic absorptivities at 254 and 280 nm were measured to obtain specic ultraviolet absorbance (SUVA) and the

anaerobic conditions electrons and protons are produced from bioconvertible substrates by bacteria attached to the anode. Subsequently the electrons and protons ow and diffuse through an external circuit and the membrane, respectively, to the cathode at which they react with oxygen to form water (Rabaey and Verstraete, 2005). A number of previous studies have recently demonstrated that MFCs can be used to harvest biologically generated electricity from organic wastes such as wastewaters (Liu et al., 2004; Min et al., 2005), sediments (Reimers et al., 2001; Tender et al., 2002), and even rhizodeposits (De Schamphelaire et al., 2008). In addition, the MFC technology has been also employed as sensors for the measurement of biochemical oxygen demand and the detection of toxic compounds (e.g., heavy metals and anthropogenic chemicals) in both natural waters and wastewaters (Chang et al., 2004; Kim et al., 2007). Reimers et al. (2001) were one of the rst to demonstrate that MFC can be adopted to extract electricity from marine environments by placing one electrode in the sediment and the other in the overlying seawater. Specic bacteria, including Geobacteraceae, were enriched on the anode where organic matter was oxidized and electrons were directly transferred to the anode under anaerobic conditions (Tender et al., 2002). However, most previous studies have paid attention to the analysis of anodophilic microbial communities (Tender et al., 2002; Holmes et al., 2004a,b) and to the enhancement of power generation from marine and freshwater sediments by: (i) adding particulate substrates (e.g., chitin and cellulose) as fuel on the anode matrix (Rezaei et al., 2007); (ii) placing the anodes inside the chambers to reduce a passivation effect (Nielsen et al., 2007); and (iii) rotating the cathode for the enhancement of oxygen availability and subsequent cathode reaction (He et al., 2007). Ryckelynck et al. (2005) have investigated the anodic mechanism associated with electricity generation, but the main focus was on the role of reduced inorganic compounds (e.g., sulde) in marine sediments. To date little effort has been directed towards quantifying and predicting the effects of anode reaction on the properties of SOM during electricity generation from sediments. It is worth noting that the anode can serve as an electron acceptor while electrochemically active bacteria oxidize organic compounds for their metabolic processes (Bond et al., 2002; Holmes et al., 2004a,b). Armed with the fact that microorganisms actively participate in the humication of organic substances in geo-environments, it can be postulated that the properties of SOM can be altered in conjunction with electricity generation via anaerobic oxidation of organic matters in the sediment MFC. The specic objective in this study was to evaluate the changes in properties of SOM stimulated by sediment MFCs operated under electricity generating conditions. The alterations of SOM were characterized with respect to its physical and chemical properties during the incubation of sediments using lab-scale current owing (closed-circuit) and nocurrent owing (open-circuit) MFCs.
2. Materials and methods 2.1. Sediment The sediment was collected from the bottom (approximately 10 cm down from the sedimentwater interface) of the Gongji stream in South Korea (37 520 N, 127 420 E).

Table 1 Physical characteristics of sediment collected from the Gongji stream. pH Electrical conductivity (mS cm1) 473 7.7b Cation exchange capacity (meq 100 g1) 9.45 0.18b Water content (%, w/w) 45.8 1.36b Organic carbon contenta (foc, %, w/w) 1.7 0.2b Soil texture (%, w/w) Sand 11.5 Silt 85.1 Clay 3.4

6.61 0.03b
a b

Determined by the WalkleyBlack method (Methods of Soil Analysis, 1996, Soil Science Society of America). Values are mean standard deviation (n 3).

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Fig. 1. Schematic diagram of the sediment MFC (the left side picture box showing a top view of the folded anode and a front view of the acrylic holder). ratios of spectroscopic absorptivities at wavelengths of 465 and 665 nm, referred to as E4/E6 ratio, were also measured using a UVvisible spectrometer (Genesys 6, Thermo Spectronic, Rochester, NY, USA). Levels of pH and the ionic strength of all aqueous samples were adjusted to approximately neutral and 0.1 M, respectively, in order to minimize the interferences on the spectroscopic absorbance measurement. Fourier transform infrared (FTIR) spectral analysis was carried out using a Nicolet 6700 FTIR spectrometer (Thermo electron, Madison, WI, USA) with KBr pellets. The molecular size and the size distribution of organic matter were analyzed by highpressure size exclusion chromatography (HPSEC) using an HPLC system (Agilent LC 1200 series, Agilent Technologies, Inc., Palo Alto, CA, USA) equipped with a Waters Protein Pak 125 SEC column (Waters, Milford, MA, USA) and a photodiode array detector (Agilent Technologies, Inc.). Relative weight-average molecular weight (Mw), relative number-average molecular weight (Mn), and polydispersivity (r) were determined as described by Zhou et al. (2000).

Holmes et al. (2004a,b) who demonstrated microbially-mediated current production using sediment MFC systems: a rapid increase in current production within the rst few days of reactor operation with no lag period, followed by a gradual decrease. The current generation with no lag time may be attributable to the abiotic oxidation of some inorganic electron donors (e.g., ferrous iron and sulde) at the anode as suggested by Ryckelynck et al. (2005). The continuous current production without any inoculum supports that the microorganisms indigenous to our freshwater sediment inherently possess the bio-catalytic activities responsible for the conversion of organic matter to electricity. Similarly, Wei and Zhang (2007) and Mathis et al. (2008) isolated the electricigenic

3. Results and discussion 3.1. Electricity generation from sediment MFCs Fig. 2 presents the current densities from the sediment MFCs with adding neither external substrates nor electron transport mediators over 120 days of operation. Immediately after the circuit connection was established, the current density sharply increased to 2.81 0.99 mA m2 (mean S.D.; n 4). A maximum current density of 20.2 0.93 mA m2 was observed at day 3, followed by the current varying within a certain range over the next 27 days. Afterwards, the currents produced from the sediment MFCs gradually decreased to ca. 2.7 mA m2. The total coulombs were determined by integrating the electrical current produced over the course of system operation (Liu et al., 2005). They were 453.5, 763.9, 932.4, and 951.0 C at days 30, 60, 90, and 120, respectively. This indicates that the majority of electrical charge was generated in the initial stage of sediment MFC runs: approximately 50% of the total amount was delivered within the rst 30 days. The overall pattern of electricity generation was analogous to that observed by

Fig. 2. Behaviors of electrical current in the sediment MFCs under closed-circuit conditions (solid circles) and voltage of the sediment MFC under open-circuit conditions (solid line). Error bars denote standard deviations.

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(also referred to as anodophilic and electrochemically-active) bacteria from natural marine sediments and demonstrated the instant electricity generation in their MFC systems augmented with isolated cultures. As opposed to the MFC systems fed with rened organic substances such as acetate and glucose as fuel (Chaudhuri and Lovley, 2003; Liu et al., 2005), the maximum current densities produced from our sediment MFCs were not sustained over time. Noting that there was no external carbon supply in this experiment, this may be ascribed to the characteristics of SOM relatively refractory to microbial utilization (Stevenson, 1982; Aiken et al., 1985) and/or the limited mass transfer of electrode reactants owing to their very slow diffusion within the sediment matrix as addressed in previous studies (Reimers et al., 2001, 2006; Hong et al., 2009). Nielsen et al. (2007) also attributed a lowered power generation to the mass transfer limitation at the anode and this problem was overcome by hydrodynamic mixing in their investigation. Meanwhile, levels of electrical current generation were fairly comparable with those previously obtained from freshwater sediment MFCs (ranging from 20 to 45 mA m2, Hong et al., 2008, 2009), but lower than those previously reported for a marine sediment MFC (Reimers et al., 2001). This may have been resulted from the low electrical conductivity in natural freshwater in comparison with that of seawater: the electrical conductivity of our overlying water was 518 mS/cm, two orders of magnitude lower than that of seawater (He et al., 2007). De Schamphelaire et al. (2008), using sediment MFC systems employed in rice planted sediments, demonstrated that stable cell potentials ranged from 695 to 800 mV under open-circuit conditions in conjunction with anodic redox potentials ranging from 240 to 340 mV (vs. SHE), indicative of the establishment of anaerobic conditions around the anode. Likewise, the cell potential under open-circuit conditions remained in the range of 840 900 mV in this study. The Eh level around the anode for the sediment incubated under open-circuit conditions was 185 20.5 mV (vs. SHE, n 3), which was similar to the level for the Gongji stream sediment (192 25.4 mV), representing the reducing environment under which obligate anaerobes such as sulfate reducers and methanogens are commonly known to be present in subsurface systems (Cookson, 1995). On the contrary, the Eh level in the vicinity of the anode for the sediment incubated under closed-circuit conditions was as high as 185 37.6 mV. Given that the anode serves as a receiver for the electrons delivered from the oxidation of organic substances rather than microbial nal electron acceptors responsible for the anaerobic reducing environment, it was not, in fact, surprising to observe the elevated Eh values in local regions around the anode in the closed-circuit sediment MFCs. This supports that the anaerobic oxidation of organic matter took place in the sediment MFC system. 3.2. Quantitative variation in SOM during electricity generation The organic carbon contents of each fractionated SOM (i.e. BP, FA, and HA) extracted from the sediments incubated under closedand open-circuit conditions along with those for the control are depicted in Fig. 3. All fractionated SOM of BP, FA, and HA for the closed-circuit sediment MFCs began to decrease slowly over the rst 30 days of operation. In comparison with the amount of electricity generated during the same period, the extent of the decrease in those SOM fractions was smaller than expected. This difference might be attributed to the release of electrons from inorganic compounds as discussed earlier. Afterwards, noticeable decreases in each of the SOM fractions were observed in conjunction with current production: approximately 56, 46, and 25% of BP, FA, and HA fractions relative to those for the control, respectively, were

Fig. 3. Changes in organic carbon content of each fractionated SOM for the sediment MFCs under closed- and open-circuit conditions. SOM for the open-circuit sediment MFC was obtained at the end of reactor operation (day 120). Control denotes SOM extracted from the original sediment collected from the Gongji stream.

diminished by the end of experiment. This supports that simplestructured and low molecular-weight SOM such as BPs associated with sediments can be more susceptible to microbial utilization than highly complex, larger, and more condensed SOM in nature such as HAs. Albeit the resistance of fulvic and humic substances to natural microbial degradation has been well-known in terrestrial and aquatic environments, several recent studies have demonstrated that a portion of humus materials can be degraded by indigenous geo-microbes (Hertkorn et al., 2002; Da Cunha-Santino and Bianchini, 2002). Our observation of SOM utilization as a carbon fuel to generate electricity was also consistent with those of previous investigators who employed similar sediment MFC systems (Tender et al., 2002; Holmes et al., 2004a,b). On the other hand, approximately 47, 43, and 18% of BP, FA, and HA fractions, respectively, were removed during the 120 days of reactor operation under open-circuit conditions (no-current ow). Similarly, Kim and Pfaender (2005) demonstrated that the organic matter associated with soils was degraded by indigenous soil microbes over a 4-month period of incubation under anaerobic conditions. Note that SOM utilization was more stimulated in the closed-circuit sediment MFC relative to the open-circuit system due to the current production. This was supported by the higher remaining organic carbon level for the open-circuit condition than that for the closed-circuit condition after 120 days of reactor operation (p value 2.5 103). It was in agreement with Hong et al. (2009) who observed that the decrease of organic carbon content in the sediment near the anode in the closed-circuit sediment MFCs was more evident than that for the open-circuit conditions. 3.3. Variation in SOM characteristics during electricity generation Table 2 summarizes variations in physical and chemical properties of SOM in response to current production as well as nocurrent production (i.e. open-circuit sediment MFC and control). As addressed in the previous section, HA fractions kept increasing with time under closed-circuit conditions relative to BP and FA. The HA fractions also increased in the open-circuit sediment MFC, but the values were less than those in the closed-circuit systems.

S.W. Hong et al. / Environmental Pollution 158 (2010) 185191 Table 2 Summary of physico-chemical property analyses for sediment organic matter. Controla Closed-circuitb 30 days Organic carbon content fractions (%, w/w) Elemental characteristics Biopolymer/humic acid Fulvic/humic acids H/C atomic ratio O/C atomic ratio Polarity index 10.86 4.04 1.51 0.68 0.76 3.51 At 254 nm At 280 nm Relative weight-average molecular weight (Mw, Da) Relative number-average molecular weight (Mn, Da) Polydispersivity (r) 9.51 7.90 14,732 1783 8.26 10.55 3.77 1.74 0.70 0.78 3.45 10.85 9.02 16,015 1832 8.74 60 days 9.80 3.46 1.61 0.73 0.80 3.43 11.20 9.28 16,061 1746 9.20 90 days 6.83 3.12 1.70 0.70 0.77 3.40 11.69 9.69 16,314 1728 9.44 120 days 6.46 2.95 1.65 0.69 0.76 3.37 12.09 10.03 16,810 1790 9.39 6.59 3.31 1.61 0.66 0.73 3.50 10.25 8.64 15,707 1692 9.28

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Open-circuitc

E4/E6 ratio SUVA (L/mg C-m) Molecule size

a b c

Original sediment sample. Sediment incubated under closed-circuit conditions for 30, 60, 90, and 120 days. Sediment incubated under open-circuit conditions for 120 days.

It has been reported that H/C and O/C ratios and the polarity index are closely related to the molecular composition and structure, functional groups, and eventually the diagenetic status of SOM (Stevenson, 1982; Aiken et al., 1985). The elemental compositions of the SOM of the sediments (e.g., ratios of H/C and O/C and polarity index) collected from the incubated reactors and the control, however, did not exhibit clear patterns in response to the electricity generation (Table 2). This may have been mainly attributable to the high ash content of our SOM (w37%, w/w) compared with the values commonly reported for soils, and this could have led to considerable errors, in particular, in oxygen content determination (Aiken et al., 1985). Compositional changes that can possibly be made in the SOM extraction and fractionation procedure as pointed by Kim and Pfaender (2005) may have also resulted in such variability observed in our analysis. Using an HPSEC, changes in relative molecule size of SOM concomitant with electricity generation were analyzed and compared to those for the open-circuit system and the control. The relative weight-average molecular weight (Mw) and polydispersity (r) increased markedly during the reactor operation under closedcircuit conditions, suggesting that macromolecules were formed along with electricity generation via anaerobic oxidation of organic matter. Such phenomena were also observed in the open-circuit sediment MFC system. These were very similar to the results of previous studies stating that macromolecule SOM was extracted from the sediments present in the very deep underground regions, representing highly reduced environments (Chin and Gschwend, 1991; Krom and Sholkovitz, 1997). Our observation of even higher values of Mw and r for the closed-circuit systems compared with those for the open-circuit system (p values 3 106 for Mw and 3.9 103 for r, respectively) indicates that the anaerobic oxidation of organic substances related to current generation may have stimulated the formation of macromolecules more evidently. Changes in the chemical properties of SOM for the closed-circuit systems were supported by a decrease in E4/E6 ratios and increases in SUVA values (p values 8.9 104 for E4/E6, 2.9 107 for SUVA at 254 nm, and 3.4 106 for SUVA at 280 nm, respectively), indicating an increased degree of humication (Table 2). It has been reported that the values of E4/E6 ratios and SUVA are closely related to the degree of condensation and the aromatic property of SOM and these can indirectly indicate its diagenetic status (Chen et al., 1977; Stevenson, 1982; Aiken et al., 1985; Weishaar et al., 2003). Our spectroscopic analyses, thus, reect that the SOM incubated under closed-circuit conditions became more aromatic and condensed compared with that for the control due to the anaerobic

oxidation of organic matter by the anode serving as an electron acceptor. Analogous characteristic alterations were also observed in the SOM incubated under open-circuit conditions. These were consistent with Kim and Pfaender (2005) with respect to the diagenetic process promoted by indigenous soil microbes particularly in anaerobic and reduced environments. The relationships between physical and chemical characteristics of SOM were evaluated by correlating values obtained from the spectroscopic measurements with the relative molecular sizes: e.g., values of SUVA at 254 and 280 nm vs. Mw and E4/E6 ratio vs. Mw (data not illustrated). They exhibited fairly good positive and negative correlations (0.83 < r2 < 0.96), indicating that the larger the molecular size, the more humied the SOM as demonstrated previously (Chen et al., 1977; Stevenson, 1982). FTIR spectra of SOM isolated from the sediments incubated under closed- and open-circuit conditions for 120 days of operations including the control are presented in Fig. 4. The absorbance peaks near 2900 cm1 ascribed to the stretching vibration of aliphatic CH bonds in CH3 and CH2 groups for the sediments incubated under closed-circuit conditions were slightly more pronounced than those for the control. This indicates that the incubated SOM exhibited more humied organic matter properties compared with the control since the stronger signal is typically

Fig. 4. FTIR spectra for the SOM samples obtained from the closed- and open-circuit sediment MFCs operated for 120 days and for the original sediment sample (control).

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observed at 2900 cm1 for HAs rather than for FAs (Senesi and Loffredo, 1999). The anaerobic oxidation of SOM was evidenced by the elevated absorbance bands near 1200 cm1 assigned to carboxylic and phenolic groups. This is in accordance with previous ndings (Lu et al., 2000; Kalbitz et al., 2003) suggesting that the increases of carboxylic and phenolic groups are probably responsible for the oxidative microbial attack on SOM. It should also be noted that the bands ranging between 1725 and 1600 cm1 became relatively stronger than those for the control, suggesting that the SOM became more like the Type I humic substance that is typical of relatively high molecular weight HA (Stevenson, 1982). Analogous to the observations for the closed-circuit conditions, apparent increases in bands around 2900, 17251600, and 1200 cm1 were observed for the open-circuit conditions. In a relevant study (Kim and Pfaender, 2005), it was demonstrated that the increases in peaks between 1650 and 1600 cm1 were attributed to an increased degree of aromatization, resulting from the alteration of SOM mediated by indigenous microorganisms under highly reduced conditions. Certainly, the values representing physical and chemical properties in the case of the control indicate that SOM of the Gongji stream sediment has been highly humied in comparison with humus materials found in other previous studies (Stevenson, 1982; Aiken et al., 1985; Senesi and Loffredo, 1999). Including the aforementioned factors (i.e. limited mass transfer and low electrical conductivity), this may be a potential reason for the relatively low levels of current production in our experiment. However, it should be noted that the diagenetic process was promoted in the sediment MFC systems, evidenced by increasing HA fractions and relative size of molecules, decreasing E4/E6 ratio, and increasing SUVA values, and it was also supported by FTIR analysis. 4. Conclusion In summary, the physico-chemical properties of SOM were considerably altered when electrical current was produced from freshwater sediments in the MFC systems. Indeed, the role of the current-harvesting anode as an electron acceptor and the anaerobic oxidation during electricity generation was supported by high Eh values and partial decomposition of SOM. Compared with the alteration of SOM under open-circuit conditions, the humication was found to be more stimulated under closed-circuit conditions, conrmed by higher HA fraction, larger molecule size, higher polydispersivity, degree of humication index, and aromaticity, and less oxidized functional groups. To the best of our knowledge, this is the rst attempt to present the possibility of articial SOM characteristic alterations along with biologically-catalyzed electricity generation similar to those observed in the natural humication processes. Based upon our observation, however, that SOM can be altered in its physical and chemical nature, the sediment MFC system may offer a potential as a new remediation technology for the contaminated geo-environment. Given that the binding characteristics of contaminants with SOM can be markedly changed by alteration of SOM properties, enhancement in their overall bioavailability or ultimate stabilization within the geo-sorbent media may be possible. Acknowledgements This work was supported by the Korea Institute of Science and Technology Institutional Research Program, and in part by the Seoul National University SIR Group of the BK21 Research Program funded by the Korean Ministry of Education & Human Resources Development and the Korean Research Foundation Grant of the Korean Government (MOEHRD, KRF-2007-331-D110403).

Appendix. Supplementary data Supplementary data associated with this article can be found in the online version at doi:10.1016/j.envpol.2009.07.022.

References
Aiken, G.R., Mcknight, D.M., Wershaw, R.L., MacCarthy, P., 1985. Humic Substances in Soil, Sediment, and Water: Geochemistry, Isolation, and Characterization. John Wiley & Sons Inc., New York. Bond, D.R., Holmes, D.E., Tender, L.M., Lovley, D.R., 2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483485. Chang, I.S., Jang, J.K., Gil, G.C., Kim, M., Kim, H.J., Cho, B.W., Kim, B.H., 2004. Continuous determination of biochemical oxygen demand using microbial fuel cell type biosensor. Biosensors & Bioelectronics 19, 607613. Chaudhuri, S.K., Lovley, D.R., 2003. Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nature Biotechnology 21, 12291232. Chen, Y.N., Senesi, M., Schnitzer, M., 1977. Information provided on humic substances by E4/E6 ratios. Soil Science Society of America Journal 41, 352358. Chin, Y.P., Gschwend, P.M., 1991. The abundance, distribution, and conguration of porewater organic colloids in recent sediments. Geochimica et Cosmochimica Acta 55, 13091317. Coates, J.D., Chakraborty, R., OConnor, S.M., Schmidt, C., Thieme, J., 2000. The geochemical effects of microbial humic substances reduction. Acta Hydrochimica et Hydrobiologica 28, 420427. Cookson Jr., J.T., 1995. Bioremediation Engineering: Design and Application. McGraw-Hill Inc., New York. Da Cunha-Santino, M.B., Bianchini, I., 2002. Humic substance mineralization in a tropical oxbow lake (Sao Paulo, Brazil). Hydrobiologia 468, 3343. De Schamphelaire, L., Van den Bossche, L., Dang, H.S., Hofte, M., Boon, N., Rabaey, K., Verstraete, W., 2008. Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environmental Science & Technology 42, 30533058. Grathwohl, P.,1990. Inuence of organic matter from soils and sediments from various origins on the sorption of some chlorinated aliphatic hydrocarbons: implications on Koc correlations. Environmental Science & Technology 24, 16871693. He, Z., Shao, H.B., Angenent, L.T., 2007. Increased power production from a sediment microbial fuel cell with a rotating cathode. Biosensors & Bioelectronics 22, 32523255. Hertkorn, N., Claus, H., Schmitt-Kopplin, Ph., Perdue, E.M., Filip, Z., 2002. Utilization and transformation of aquatic humic substances by autochthonous microorganisms. Environmental Science & Technology 36, 43344345. Holmes, D.E., Bond, D.R., Lovley, D.R., 2004a. Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Applied Environmental Microbiology 70, 12341237. Holmes, D.E., Bond, D.R., ONeill, R.A., Reimers, C.E., Tender, L.R., Lovley, D.R., 2004b. Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microbial Ecology 48, 178190. Hong, S.W., Chang, I.S., Choi, Y.S., Kim, B.H., Chung, T.H., 2009. Responses from freshwater sediment during electricity generation using microbial fuel cells. Bioprocess & Biosystems Engineering 32, 389395. Hong, S.W., Kim, H.J., Choi, Y.S., Chung, T.H., 2008. Field experiments on bioelectricity production from lake sediment using microbial fuel cell technology. Bulletin of the Korean Chemical Society 29, 21892194. Huang, W.L., Weber, W.J., 1997. A distributed reactivity model for sorption by soils and sediments. 10. Relationships between desorption, hysteresis, and the chemical characteristics of organic domains. Environmental Science & Technology 31, 25622569. Kalbitz, K., Schwesig, D., Schmerwitz, J., Kaiser, K., Haumaier, L., Glaser, B., Ellerbrock, R., Leinweber, P., 2003. Changes in properties of soil-derived dissolved organic matter induced by biodegradation. Soil Biology & Biochemistry 35, 11291142. Kim, H.S., Pfaender, F.K., 2005. Effects of microbially mediated redox conditions on PAHsoil interactions. Environmental Science & Technology 39, 91899196. Kim, M., Hyun, M.S., Gadd, G.M., Kim, H.J., 2007. A novel biomonitoring system using microbial fuel cells. Journal of Environmental Monitoring 9, 13231328. Krom, M.D., Sholkovitz, E.R., 1997. Nature and reactions of dissolved organic matter in the interstitial waters of marine sediments. Geochimica et Cosmochimica Acta 41, 15651573. Kruge, M.A., Mukhopadhyay, P.K., Lewis, C.F.M., 1998. A molecular evaluation of contaminants and natural organic matter in bottom sediments from western Lake Ontario. Organic Geochemistry 29, 17971812. Liu, H., Cheng, S.A., Logan, B.E., 2005. Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environmental Science & Technology 39, 658662. Liu, H., Ramnarayanan, R., Logan, B.E., 2004. Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environmental Science & Technology 38, 22812285. Loffredo, E., DOrazio, V., Brunettti, G., Senesi, N., 1999. Adsorption of chlordane onto humic acids from soils and pig slurry. Organic Geochemistry 30, 443451. Lu, X.Q., Hanna, J.V., Johnson, W.D., 2000. Source indicators of humic substances: an elemental composition, solid state C-13 CP/MAS NMR and Py-GC/MS study. Applied Geochemistry 15, 10191033.

S.W. Hong et al. / Environmental Pollution 158 (2010) 185191 Mathis, B.J., Marshall, C.W., Milliken, C.E., Makkar, R.S., Creager, S.E., May, H.D., 2008. Electricity generation by thermophilic microorganisms from marine sediment. Applied Microbiology & Biotechnology 78, 147155. Min, B., Kim, J.R., Oh, S.E., Regan, J.M., Logan, B.E., 2005. Electricity generation from swine wastewater using microbial fuel cells. Water Research 39, 49614968. Nielsen, M.E., Reimers, C.E., Stecher, H.A., 2007. Enhanced power from chambered benthic microbial fuel cells. Environmental Science & Technology 41, 78957900. Rabaey, K., Verstraete, W., 2005. Microbial fuel cells: novel biotechnology for energy generation. Trends in Biotechnology 23, 291298. Reimers, C.E., Girguis, P., Stecher III, H.A., Tender, L.M., Ryckelynck, N., 2006. Microbial fuel cell energy from an ocean cold seep. Geobiology 4, 123136. Reimers, C.E., Tender, L.M., Fertig, S., Wang, W., 2001. Harvesting energy from the marine sediment-water interface. Environmental Science & Technology 35, 192195. Rezaei, F., Richard, T.L., Brennan, R.A., Logan, B.E., 2007. Substrate-enhanced microbial fuel cells for improved remote power generation from sedimentbased systems. Environmental Science & Technology 41, 40534058. Ryckelynck, N., Stecher III, H.A., Reimers, C.E., 2005. Understanding the anodic mechanism of a seaoor fuel cell: interactions between geochemistry and microbial activity. Biogeochemistry 76, 113139.

191

Senesi, N., Loffredo, E., 1999. The chemistry of soil organic matter. In: Sparks, D.L. (Ed.), Soil Physical Chemistry. CRC Press, Boca Raton, FL, pp. 331332. Stevenson, T.G., 1982. Humus Chemistry, Genesis, Composition, and Reactions. John Wiley & Sons Inc., New York. Tender, L.M., Reimers, C.E., Stecher, H.A., Holmes, D.E., Bond, D.R., Lowy, D.A., Pilobello, K., Fertig, S.J., Lovley, D.R., 2002. Harnessing microbially generated power on the seaoor. Nature Biotechnology 20, 821825. Wei, D., Zhang, X., 2007. Current production by a deep-sea strain Shewanella sp. DS1. Current Microbiology 55, 497500. Weishaar, J.L., Aiken, G.R., Bergamaschi, B.A., Fram, M.S., Fujii, R., Mopper, K., 2003. Evaluation of specic ultraviolet absorbance as an indicator of the chemical composition and reactivity of dissolved organic carbon. Environmental Science & Technology 37, 47024708. Xing, B., 2001. Sorption of naphthalene and phenanthrene by soil humic acids. Environmental Pollution 111, 303309. Zhou, Q.H., Cabaniss, S.E., Maurice, P.A., 2000. Considerations in the use of high-pressure size exclusion chromatography (HPSEC) for determining molecular weights of aquatic humic substances. Water Research 34, 35053514.