Bioresource Technology 143 (2013) 25–31
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Ammonia recycling enables sustainable operation of bioelectrochemical systems Ka Yu Cheng a,⇑, Anna H. Kaksonen a, Ralf Cord-Ruwisch b a b
CSIRO Land and Water, Floreat, WA 6014, Australia School of Biological Science and Biotechnology, Murdoch University, WA 6150, Australia
h i g h l i g h t s
g r a p h i c a l a b s t r a c t
Anolyte acidiﬁcation (pH <5.5)
0.25CO2 Gas Liquid
0.25 CH2O 0.25 H2O
severely inhibited current generation. Ammonium selectively migrated across a cation exchange membrane to the catholyte. Recycling the ammonia to anolyte neutralized the acidity and sustained current. Ammonia recycling was achieved without using external carrier gases.
100 >98% as NH4+
75 50 25
>84% as freeNH3
a r t i c l e
i n f o
Article history: Received 28 March 2013 Received in revised form 22 May 2013 Accepted 25 May 2013 Available online 31 May 2013 Keywords: Microbial fuel cells Microbial electrolysis cells Proton gradient pH Split Cation exchange membrane
a b s t r a c t Ammonium ðNHþ 4 Þ migration across a cation exchange membrane is commonly observed during the operation of bioelectrochemical systems (BES). This often leads to anolyte acidiﬁcation (pH <5.5) and complete inactivation of bioﬁlm electroactivity. Without using conventional pH controls (dosage of alkali or pH buffers), the present study revealed that anodic bioﬁlm activity (current) could be sustained if recycling of ammonia (NH3) was implemented. A simple gas-exchange apparatus was designed to enable continuous recycling of NH3 (released from the catholyte at pH >10) from the cathodic headspace to the acidiﬁed anolyte. Results indicated that current (110 mA or 688 A m3 net anodic chamber volume) was sustained as long as the NH3 recycling path was enabled, facilitating continuous anolyte neutralization with the recycled NH3. Since the microbial current enabled NHþ 4 migration against a strong concentration gradient (10-fold), a novel way of ammonia recovery from wastewaters could be envisaged. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction Bioelectrochemical systems (BES) have shown promise for the conversion of organic compounds in wastewaters into valuables (e.g., electricity, fuel gases, chemicals, etc.) (Logan et al., 2008; Rabaey and Verstraete, 2005; Rittmann, 2008). Arguably, the microbial catalyzed anodic reaction is the most critical reaction
⇑ Corresponding author. Tel.: +61 (8) 9333 6158; fax: +61 (8) 9333 6211. E-mail address: [email protected]
(K.Y. Cheng). 0960-8524/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biortech.2013.05.108
in a BES process as it transforms the chemical energy captured in the organics directly into electrical energy. Typically, this reaction not only produces electrons, but also liberates protons (H+). For instance, anodic oxidation of one mole acetate liberates nine mole H+ and eight mole electrons according to the following equation (Schroder, 2007):
CH3 COO þ 4H2 O ! 2HCO3 þ 9Hþ þ 8e Since the electrons are continuously scavenged by the anode, the liberated H+ accumulates and leads to anolyte acidiﬁcation (Marcus et al., 2011). This has been shown to severely inhibit the
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catalytic activity of anodic bioﬁlms and consequently leading to a complete shutdown of the BES (Cheng et al., 2010; Clauwaert et al., 2007, 2008). In general, a pH neutral condition (pH 7, i.e., [H+] = 107 mol L1) is essential to sustain optimal anodic microbial activities (He et al., 2008; Patil et al., 2011). In theory, pH neutral anodic condition can be sustained if the requirement of cation migration (to establish charge balance) is satisﬁed exclusively by proton migration, resulting in the proton ﬂux from anode to cathode being equal to the electron ﬂow and the proton generation at the anode. However, in reality cations other than protons (Na+, K+, Ca2+, Mg2+, NHþ 4 ) are available in much higher concentrations and will hence tend to migrate instead of protons. The higher the concentration of other cations is relative to protons, the lower is the likelihood of proton migration. Under typical experimental conditions the concentration of alkali cations such as Na+ is orders of magnitudes higher than that of protons resulting in the migration of Na+ from anode to cathode (Harnisch et al., 2008; Rozendal et al., 2006a). This effect has been suggested to be industrially exploited for the production of caustic soda (Rabaey et al., 2010). In laboratory trials, the problem of anolyte acidiﬁcation is often masked by the dosage of pH buffer or alkali (Cheng et al., 2010; Rozendal et al., 2008a). However, these pH control strategies are not sustainable as pH controlling chemicals must be externally added to the process. To approach self-sustaining pH control for CEM-BES without using external chemicals, the migrating cation species across the CEM should possess four properties: (1) it must be an alkaline species neutralizing the excess protons in the anolyte; (2) upon reacting with proton it becomes a cation that migrates across the CEM to the catholyte to maintain charge balance; (3) in the catholyte, it readily dissociates and releases the proton and hence replenishes the proton consumed in the cathodic reaction; and (4) upon releasing the proton in the catholyte, the species can be recycled for neutralizing the anolyte again (Cord-Ruwisch et al., 2011). Amongst all cation species typically found in wastewaters (e.g., þ Na+, K+, Ca2+, Mg2+, NHþ 4 ), ammonium ðNH4 Þ is the only species that fulﬁls all the above criteria. It has a characteristic acid-dissociation
constant (pKa value) of 9.25 (25 °C). Hence, once it has migrated across a CEM to the catholyte, where the localized pH exceeds 9.25, it dissociates predominantly as free volatile ammonia (NH3) which can be recovered as a gas (Fig. 1). The concept of using NHþ 4 as a proton shuttle in a CEM-equipped BES (CEM-BES) has been evaluated in our recent work (Cord-Ruwisch et al., 2011). The ammonia recycling was achieved by continuously stripping the catholyte with nitrogen (N2), which was directed through the acidiﬁed anolyte to close the loop. N2 was used to maintain the anaerobic condition required for the microbial anodic reaction. However, N2 stripping is impractical as it incurs substantial energy input and creates large volume of low-value off-gas. In order to use the very effective principle of ammonia recycling for the sustainable operation of BES, a simple low energy input approach is required. This work examined a new approach to sustain the current generation in a CEM-BES by internal ammonia recycling without using N2 stripping. The idea is based on the well-known phenomenon where under anaerobic and highly reducing conditions (e.g., 6500 mV vs. Ag/AgCl), a BES cathode produces hydrogen gas. This gas stream is in principle a vector that could help driving the volatilized ammonia out of the cathodic half cell (Liu et al., 2005; Logan et al., 2008; Rozendal et al., 2006b, 2008b). The aim of this study was to develop an effective way of sustaining BES operation by maintaining suitable anodic pH levels using ammonia from the cathode as the alkalinity carrier. In contrast to our previous work (Cord-Ruwisch et al., 2011), a more efﬁcient (10-fold higher current density) anodic bioﬁlm was used to demonstrate the concept of ammonia recycling in a BES.
2. Methods 2.1. Bioelectrochemical system conﬁguration and process monitoring A two-chamber CEM-BES was used in this study. It was made of transparent Perspex and has a similar conﬁguration as the one described in an earlier work (Cheng et al., 2008). The two half cells
0.25CO2 Gas Liquid
0.25 CH2O 0.25 H2O
Bio-anode 100 >98% as NH4+
75 50 25
>84% as freeNH3
pH Fig. 1. The principle of using ammonium/ammonia as a proton shuttle in a CEM-BES. Here, the cathode is anaerobically operated enabling abiotic hydrogen gas formation. At neutral anolyte pH (pH 6.5–7.5), ammonia predominantly exists as NHþ 4 , whereas free volatile NH3 dominates in the catholyte (pH >10).
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were of equal volume and dimension (316 mL, 14 12 1.88 cm). They were physically separated by a cation exchange membrane (CMI-7000, Membrane International Inc.) which has a surface area of 168 cm2. Both chambers were ﬁlled with conductive granular graphite (3–6 mm diameter), which reduced the void volume of the working chamber from 316 to 160 mL. A graphite rod (diameter 5 mm) was inserted into each half cell to allow the electric contact between the graphite granules and the external circuit. In this study, only one half cell was inoculated with bacteria and was operated as an anodic half cell, which is termed here as the working chamber. The other half cell (cathodic) is termed as the counter chamber. The graphite granules inside the working chamber (i.e. working electrode) was polarized against a silver–silver chloride (Ag/ AgCl) reference electrode (saturated KCl) at a potential of 300 mV by using a potentiostat (Model No. 362, EG&G, Princeton Applied Research, Instruments Pty. Ltd.). This potential was selected as it facilitated an effective anodic acetate oxidation that could signiﬁcantly acidify the anolyte if no effective pH control was implemented. The Ag/AgCl electrode was mounted inside the working chamber at a distance of less than one cm away from the working electrode. All electrode potentials (mV) in this article refer to values against the Ag/AgCl reference (ca. +197 mV vs. standard hydrogen electrode, (Bard and Faulkner, 2001)). The working electrolyte redox potential and the pH of both working and counter electrolyte were continuously monitored. A computer program (LabVIEW™, National Instrument) was developed to continuously control and monitor the bioprocess. An analog input/output data acquisition card (National Instrument™) was used to interface between the computer and the potentiostat. The BES current was monitored directly from the potentiostat. The electrode potentials, redox potentials and pH voltage signals were recorded at ﬁxed time intervals and all data were regularly logged into an Excel spreadsheet.
2.2. Process start-up and general operation To start up the BES process, the working chamber was inoculated with returned activated sludge collected from a municipal sewage treatment plant (Subiaco, Perth, WA) (ﬁnal mixed liquor suspended solid concentration was ca. 2 g L1). A synthetic wastewater medium with a limited pH buffering capacity was used as both the working and counter electrolyte throughout the study. It consisted of (mg L1): NH4Cl 125, NaHCO3 125, MgSO47H2O 51, CaCl22H2O 300, FeSO47H2O 6.25, and 1.25 mL L1 of trace element solution, which contained (g L1): ethylene–diamine tetraacetic acid (EDTA) 15, ZnSO47H2O 0.43, CoCl26H2O 0.24, MnCl24H2O 0.99, CuSO45H2O 0.25, NaMoO42H2O 0.22, NiCl26H2O 0.19, NaSeO410H2O 0.21, H3BO4 0.014, and NaWO42H2O 0.050 (Cheng et al., 2010). The working electrolyte was supplemented with yeast extract (50 mg L1 ﬁnal concentration) as bacterial growth supplement during the initial start up period (ca. 2 weeks). During this period, the entire medium was refreshed once every 4 days. Acetate was used as the sole electron donor substrate for the anodic bioﬁlm. A known amount of acetate standard solution (1 M) was added to the working electrolyte to obtain a desired acetate concentration (ranged from 1 to 50 mM). Unless stated otherwise, each half cell was hydraulically linked to a separate glass recirculation bottle, which accommodated the extra volume of electrolyte; 0.5 and 0.7 L of anolyte and catholyte were continuously recirculating through the anodic and catholyte half cell, respectively, at a rate of 6 L h1. The CEM-BES was operated in batch mode at ambient temperature (25 ± 3 °C).
2.3. Ammonia recycling apparatus and its integration with the CEMBES An ammonia-recycling apparatus was designed to enable recycling of ammonia from the cathodic headspace to the anolyte (Fig. 2). It was constructed by gluing two 390 mL modiﬁed polyethylene terephthalate-made plastic containers together side by side with a common open window between them (5 4 cm). The two containers were hydraulically separated from each other but were hydraulically connected with the anodic and cathodic half cell of the BES, respectively. As such, one container received the anolyte recirculation stream and the other the catholyte recirculation stream. The common window was sealed with a gas permeable ﬁber cloth (6 5 cm), which was mounted at the anodic side and was continuously trickled with the anolyte. After trickling through the cloth, the anolyte was recirculated back to the BES anode. As both the inﬂux and outﬂux rates of anolyte were identical (6 L h1), a ﬁxed volume of anolyte (ca. 50 mL) was always retained in the apparatus. At the cathodic side of the apparatus, the catholyte from the BES cathode was continuously sprinkled over the catholyte reservoir (ca. 50 mL) to facilitate ammonia volatilization within the cathodic container. Since the cathodic BES half cell was gas-tight, any build up of gas pressure would help drive the ammonia-containing gas in the cathodic container through the gas permeable cloth and the laminar ﬂow of anolyte. This facilitated the dissolution of ammonia gas into the acidiﬁed anolyte. After retroﬁtted with the gas exchange apparatus, the total volume of both the working and counter electrolyte was reduced to about 220 mL. The recirculation rates of both the anolyte and catholyte were kept at 6 L h1, corresponding to a hydraulic retention time of approximately 30 s for both anolyte and catholyte in the apparatus. 2.4. Experimental procedures Experiments were conducted to ﬁrst investigate the effect of anolyte acidiﬁcation on the anodic bioﬁlm activity (current production). No ammonia recycling was implemented during this period. The initial bioﬁlm establishment was facilitated by actively controlling the anolyte pH at around seven using feedback dosing of NH4OH (1 M). The dosage was computer recorded to obtain the NH4OH application rate. The catholyte was not pH controlled and hence it would become signiﬁcantly alkaline, facilitating the NH3 volatilization at the cathodic half cell. No aeration was provided to the catholyte. At the beginning of each batch run, the ammonia recycling apparatus was ﬂushed with N2 to obtain the anaerobic condition. The effect of anolyte acidiﬁcation was examined by comparing the current obtained with or without active dosing of NH4OH. Coulombic efﬁciencies of the anodic acetate oxidation (5 mM) under pH neutral and acidiﬁed conditions were also compared (Logan et al., 2006). At selected time intervals, aliquots (1 mL) of anolyte and catholyte were sampled for chemical analysis. To demonstrate the effect of recycling the ammonia containing off-gas from the cathode to the anodic half cell, the catholyte in the recirculating bottle was continuously stripped with a pure nitrogen gas stream (1 L min1) which was then introduced back into the anolyte, completing an NH3 recycling loop. Current, anolyte pH, acetate, ammonium, sodium and potassium concentrations were recorded over a period of two days with or without NH3 looping. To verify whether the ammonia transfer from the cathodic headspace to the anolyte could sustain the anodic bioﬁlm activity, the BES was retroﬁtted with the ammonia recycling apparatus as described above. The effect of looping (i.e. gas exchanged was enabled via gas permeable cloth) on electrolyte pH and current was evaluated over an operational period of about 100 h.
K.Y. Cheng et al. / Bioresource Technology 143 (2013) 25–31
H2 (g) + CO2 (g)
H +(aq) NH 3 Scrubber (Fibre Cloth) NH3 (g) +H2 (g)
Ammonia Recycling Apparatus
Electrical current Anodic Chamber
Bioelectrochemical System Cathode
H2 (g) H+ (aq) NH 3 (aq)
Cation Exchange Membrane Fig. 2. Schematic of the proposed ammonia recycling apparatus connected in-series with a CEM-BES. The process is anaerobic and hence favoring cathodic hydrogen production. Diagram not drawn to scale.
2.5. Chemical analysis
pH Controlled with NH4OH
No pH Control
8 Current Anolyte pH Catholyte pH Acetate
50 0 200
80 NH 4OH Added NH 4+-N Anolyte NH 4+-N Catholyte
120 96 96 Time (h)
NH 4+-N (mM)
Cummulative NH 4OH Added (mmole)
pH/ Acetate Conc. (mM)
Liquid samples taken from the BES were immediately ﬁltered through a 0.2 lm ﬁlter (0.8/0.2 lm SuporÒ Membrane, PALLÒ Life Sciences) and were stored at 4 °C prior analysis. Acetate in the samples was analyzed using a Dionex ICS-3000 reagent free ion chromatography (RFIC) system equipped with an IonPacÒ AS18 4 250 mm column (Cheng et al., 2012). Ten microliters of the
Fig. 3. Effect of continuous anodic pH control by ammonium hydroxide addition on the current of the BES and ammonium migration to the cathode. At time zero, the anodic chamber was inoculated with bioﬁlm fragments from a microbial fuel cell operated with acetate. Arrows 1 and 2 indicate additions of sodium acetate: 0.5 mmol (1 mM) and 2 mmol (4 mM), respectively.
sample was injected into the column. Potassium hydroxide was used as an eluent at a ﬂow rate of 1 mL min1. The eluent concentration was 12–45 mM from 0 to 5 min, 45 mM from 5 to 8 min, 45–60 mM from 8 to 10 min and 60–12 mM from 10 to 13 min. Ammonium (NHþ 4 –N), potassium and sodium in the ﬁltered samples were measured with the same RFIC with a IonPacÒ CG16, CS16, 5 mm column. Methanesulfonic acid was used as an eluent with a ﬂow rate of 1 mL min1. The eluent concentration was 30 mM for 29 min. The temperature of the two columns was maintained at 30 °C. Suppressed conductivity was used as the detection signal (ASRS ULTRA II 4 mm, 150 mA, AutoSuppressionÒ recycle mode).
3. Results and discussion 3.1. Anolyte acidiﬁcation severely limited current generation The reactor described above was started up and operated to quantify the effect of pH drifts typically observed in CEM-equipped bioelectrochemical systems. After approximately two days of incubation, anodic current evolved gradually indicating that the microbial inoculum in the anodic chamber became electrochemically active. As expected, the current generation coincided with an acidiﬁcation of the anolyte (pH 5.5) and an alkalization of the catholyte (pH 13), respectively (Fig. 3A). As the working electrode (bioﬁlm anode) was maintained at a constant potential (300 mV) and the substrate was not limiting (acetate, >10 mM), the observed current decline which followed the anodic acidiﬁcation indicated that the low pH had suppressed the anodic activity of the bioﬁlm. Similar observation has been reported by others (Cheng et al., 2010; Harnisch and Schroder, 2009; He et al., 2008; Sleutels et al., 2010).
K.Y. Cheng et al. / Bioresource Technology 143 (2013) 25–31
No NH 3 Recycle
Cumulated NH4OH (mmole)
40 (C) 20
Time (h) 20
100 50 0
0 13 (B) 11
200 Current (mA)
 Coulombic Recovery = 36 %
Fig. 4. Current production from a 5 mM acetate spike (dotted vertical lines) in the presence (0–22 h) and absence (22–40 h) of anodic pH control by automated ammonium hydroxide addition. The anode was potentiostatically controlled at 300 mV vs. Ag/AgCl.
3.2. Effect of anolyte neutralization on current production The pH neutralization by the traditional NaOH addition was replaced by using an ammonium hydroxide solution. Neutralizing the anolyte acidity to pH 7 by dosing ammonium hydroxide immediately resumed current production (at 110 h, Fig. 3). Prolonged current generation necessitated the demand of ammonium hydroxide, suggesting that this pH control approach could effectively sustain the anodic activity of the bioﬁlm. As long as the anolyte pH was maintained neutral, the established bioﬁlm could effectively catalyze acetate oxidation with a good coulombic recovery (>80%) (Fig. 4). The intermittent dosing of ammonium hydroxide into the anolyte resulted in a gradual increase of ammonium concentration in the catholyte, reaching a level of about 90 mM NHþ 4 –N (Fig. 3B). Although ammonium hydroxide was continuously added to the anolyte, its concentration stayed approximately 10-fold lower than in the catholyte (Fig. 3B). Clearly, the ammonium kept migrating against its concentration gradient from the anolyte to the catholyte across the cation exchange membrane. Of the amount of ammonium migrated from the anolyte to the catholyte, 88.7% of the ammonium was lost from the catholyte (data not shown). Such a loss was most likely due to the high catholyte pH (>11) that favors the dissociation of ammonium as free ammonia and its volatilization from the catholyte. 3.3. Effect of NH3 recycle from cathode to anolyte via N2 gas stream To quantify to what extent recycling the migrated ammonium from catholyte back to the anolyte could overcome the detrimental anolyte acidiﬁcation, N2 gas was purged in series through the catholyte and then through the anolyte (Fig. 5). Before allowing the N2 ﬂow, the CEM-BES responded to the addition of an acetate spike (10 mM) not only by producing an anodic current (Fig. 5A) and degrading acetate, but also, as in Fig. 4, by an associated pH drop in the anolyte (Fig. 5B). As expected, the anolyte acidiﬁcation had slowed down the anodic activity of the bioﬁlm and the current declined signiﬁcantly even though acetate was still present in excess (>3 mM). When switching on the N2 ﬂow (21–27 h, Fig. 5B), the current and acetate degradation resumed as explained the rise in
NH 4+ -N (mM)
Coulombic Recovery = 81 %
13 Acetate Catholyte pH Anolyte pH
5 7 0 80
60 40 20 0 80
NH3 Recycled No NH3 Recycle
Na+(Catholyte) K+ (Catholyte)
Neutral Anolyte pH 200 (A)
Fig. 5. Effect on the current generation of the CEM-BES of recycling ammonia from the cathode to the anolyte via a gas stream. Legend: (1) acetate was added to the anolyte; (2) purged N2 through the catholyte and the off-gas was introduced directly into the anolyte (N2 ﬂow rate was about 1 L min1); (3) sodium acetate was added to the anolyte; (4) nitrogen purging was terminated; (5) acetate was added to the anolyte.
pH caused by the alkalinity transfer from the catholyte (as ammonia) to the anolyte. The BES now operated sustainably without a marked drift in anolyte pH. Repeating the stopping and starting of ammonia exchange by N2 transfer showed the same principal effect. Further, the result also suggested that cations other than ammonium (sodium and potassium) also migrated across the CEM from the anolyte to the catholyte, but unlike ammonium which could be removed from the catholyte as a gas, both sodium and potassium accumulated in the catholyte during current production (Fig. 5C and D). This observation clearly highlights the uniqueness of ammonium as both the charge-balancing species and recyclable alkalinity carrier in a BES system. 3.4. Diffusional ammonia transfer from cathode to anode Using nitrogen to strip off the ammonia gas from the catholyte and recycle the ammonia containing nitrogen gas stream into the anolyte incurs extra energy to the extent where the energetic sustainability of a BES would become questionable. Further, in BES where H2 is produced at the cathode, this valuable fuel gas would be lost via dilution with N2. Instead of continuously purging N2 through the cell, the recycling of ammonia could in theory be done by allowing the ammonia gas to vent from the catholyte and diffuse back to the anolyte. For this purpose a sufﬁciently large ‘‘gas exchange window’’ between the gas space of anodic and cathodic
K.Y. Cheng et al. / Bioresource Technology 143 (2013) 25–31 Un-Loop Ac 1
NH3-Loop Ac 3
system was anaerobic and the cathode was maintained at highly reducing (negative) potentials (<2 V vs. Ag/AgCl, Fig. 6C). This gas was released from the system via the vent (Fig. 2), and may have participated in stripping of the NH3 from the catholyte to the gaseous phase. Hydrogen transfer from the cathodic chamber to the ammonia recycling apparatus can be explained by minute bubbles visible in the catholyte. However, due to its poor solubility compared to ammonia the transfer of hydrogen to anodic chamber is expected to be minimal. 3.5. Practical considerations
Time (h) Fig. 6. Effect of looping the gas-permeable path in the ammonia recycling apparatus on current production by the CEM-BES. Anodic potential was controlled at 300 mV vs. Ag/AgCl throughout the experiment. The BES was operated under anaerobic condition. Ac 1–4 represent additions of 10 (45 mM), 5 (23 mM), 9 (41 mM) and 9 (41 mM) mmol of sodium acetate to the anolyte, respectively.
chamber would need to be used. This could be accomplished in a number of ways, including the use of a gas permeable membrane. To test whether diffusional gas exchange between the gas spaces of anodic and cathodic chamber enable adequate ammonia transfer, a separate apparatus was designed to act as the extended gas space of the two chambers (Fig. 2). The anolyte recycle was used to wet a vertically mounted gas permeable cloth that acted as the gas diffusion window, while the catholyte recycle was via a spray to facilitate NH3 transfer from the alkaline catholyte to the gas phase (Fig. 2). The vented NH3 in the gas phase of the apparatus is expected to readily dissolve in the water saturated cloth which served as an ammonia scrubber. The anolyte acidity was thus neutralized with the aim of sustaining the anodic microbial activity. Below the effectiveness of this ammonia looping technique for sustaining the microbe-driven current of a CEM-BES is described (Fig. 6). With the ammonia recycling apparatus (Fig. 2) disconnected, the CEM-BES responded to the addition of an acetate spike (10 Mmoles) by instantly producing an anodic current and a decrease in anolyte pH to about 5.8. At this stage, another acetate addition (Ac 2 in Fig. 6) did not resume the current demonstrating again that the CEM-BES had become inactive due to acidiﬁcation of the anolyte. As soon as the gas exchange by the described apparatus was enabled, the anolyte pH was neutralized almost immediately (Fig. 6B) allowing sustained current close to the maximum rate of this particular anodic bioﬁlm as long as the acetate was available. Renewed acetate addition at 55 h resumed the current. When the gas exchange between anolyte and catholyte was interrupted (78 h) the anodic current could not be sustained again due to the anolyte acidiﬁcation. By merely allowing the gas diffusion window between anodic and cathodic chamber (at 96 h), continued current production could be sustained for several days as long as the anodic substrate (acetate) was not limiting (data not shown). It was noticed that a net gas pressure build-up in the system occurred, presumably due to cathodic hydrogen production as the
The experiments suggest that sustained current production in a CEM-BES is possible only if the anodic bioﬁlm was operated under a neutral pH condition. Maintaining such a condition is difﬁcult particularly for systems designed for high current output (Marcus et al., 2011; Picioreanu et al., 2010). This study demonstrated that without using conventional active pH control methods (e.g. regular dosage of alkali hydroxide or pH buffering chemicals), a relatively high anodic current (110 mA; 688 A m3 net anodic chamber volume; 500 A m3 total anolyte volume) could be sustained if a simple ammonia recycle via gas diffusion was implemented. Although the diffusivity of protons is about ﬁve times higher than that of ammonium (9.31 105 vs. 1.96 105 cm2 s1 (Vanysek, 2000)), in the absence of ammonium the current is limited by the slow proton ﬂux because of the low proton concentrations (106 M at pH 6). The presence of about 10 mM (102 M) of ammonium to the anode can enable an up to 104 times higher cation ﬂux from anode to cathode and hence a higher current. While high ionic ﬂuxes can also be guaranteed with the addition of other cations such as sodium, as is the case when using traditional sodium hydroxide based pH control of the anolyte (Cheng et al., 2008, 2010), a dosage of sodium hydroxide requires substantial energy costs (Cord-Ruwisch et al., 2011) and intermittent renewal of the catholyte due to sodium accumulation (Rabaey et al., 2010). Nevertheless, the proposed concept has several constraints that may limit its practical use. For instance, this approach may only be applied in a microbial electrolysis mode as the production of hydrogen is essential to create a carrier stream to bring the ammonia from the catholyte to the anolyte. The high pH environment (>pH 9.25) required for the shift of NHþ 4 /NH3 equilibrium in favor of ammonia stripping may also limit the use of this approach for (cathodic) bioelectrosynthesis, which typically occurs under the neutral pH condition. Further, the use of ammonia recycling in a BES can be unacceptable if the presence of ammonia in the anolyte is undesirable (e.g. wastewater treatment). If relying on ammonia as the proton carrier in a BES, the use of N2 as the recycling agent of ammonia has been described as a proof of concept (Cord-Ruwisch et al., 2011). However, due to costs and dilution of cathodic hydrogen the use of external N2 is likely to be impractical for most applications. The gas exchange apparatus described in the present study showed immediate effects on anolyte neutralization and the production of anodic current, suggesting that the current was not limited by the rate of ammonia recycle but by the rate of microbial electron delivery to the anode. Accordingly, simpler and smaller gas exchange devices could be designed. Further research is warranted to explore how efﬁcient a BES process with the proposed NH3 recycling mechanism could sustain cathodic hydrogen production. A further step towards implementing low energy ammonia recycle as a build-in proton carrier in BES could be the use of a gas permeable membrane between anolyte and catholyte or to develop and use a gas permeable cation exchange membrane. Such a system would not depend on the physical movement of anolyte and catholyte also should enable a more effective low-energy NH3 recycle. To what extent membrane-free BES could proﬁt from
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ammonium as proton carriers is yet to be investigated. It is conceivable that by using gas permeable membranes as part of the ion exchange separator (e.g. a CEM that is also gas permeable) the ammonia recycle could become a seamless feature of a BES. The presented work shows that ammonia readily migrates from the anode to the cathode against a rather strong diffusion gradient (10-fold, Fig. 3B). In principle that would mean that ammonium containing wastewaters treated in the BES anode would be likely to lose ammonia by migration to the catholyte. If this effect can be used to concentrate up ammonia by 10 or even 100-fold a novel way of ammonia recovery from wastewater could be envisaged. 4. Conclusions Overall, this study demonstrates that by continuously recycling ammonia from the catholyte to the anolyte in a CEM-BES, neutral pH condition desirable for the anodic bioﬁlm could be maintained without using conventional pH control methods (e.g. regular dosage of alkaline hydroxide or pH buffering chemicals). The use of the proposed gas exchange device was effective to recycle the ammonia without using energy-intensive N2 stripping of the catholyte. This approach of pH control in BES systems has not been reported elsewhere, and it has the potential to be further developed to achieve recovery of ammonia from wastewaters. Acknowledgement This work was funded by the CSIRO Ofﬁce of the Chief Executive (OCE) Postdoctoral Fellowship and CSIRO Water for a Healthy Country Flagship. References Bard, A.J., Faulkner, L.R., 2001. Electrochemical Methods: Fundamentals and Applications. John Wiley & Sons, Inc., New York, USA. Cheng, K.Y., Ho, G., Cord-Ruwisch, R., 2008. Afﬁnity of microbial fuel cell bioﬁlm for the anodic potential. Environ. Sci. Technol. 42, 3828–3834. Cheng, K.Y., Ho, G., Cord-Ruwisch, R., 2010. Anodophilic bioﬁlm catalyzes cathodic oxygen reduction. Environ. Sci. Technol. 44, 518–525. Cheng, K.Y., Ginige, M.P., Kaksonen, A.H., 2012. Ano-cathodophilic bioﬁlm catalyzes both anodic carbon oxidation and cathodic denitriﬁcation. Environ. Sci. Technol. 46, 10372–10378. Clauwaert, P., Van Der Ha, D., Boon, N., Verbeken, K., Verhaege, M., Rabaey, K., Verstraete, W., 2007. Open air biocathode enables effective electricity generation with microbial fuel cells. Environ. Sci. Technol. 41, 7564–7569.
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