Biocathode in microbial electrolysis cell; present status and future prospects

Renewable and Sustainable Energy Reviews 47 (2015) 23–33

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Renewable and Sustainable Energy Reviews journal homepage: www.elsevier.com/locate/rser

Biocathode in microbial electrolysis cell; present status and future prospects Tahereh Jafary a, Wan Ramli Wan Daud a,b, Mostafa Ghasemi a,n, Byung Hong Kim a, Jamaliah Md Jahim a,b, Manal Ismail a,b, Swee Su Lim a a b

Fuel Cell Institute, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia Department of Chemical and Process Engineering, Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor, Malaysia

art ic l e i nf o

a b s t r a c t

Article history: Received 26 August 2014 Received in revised form 8 January 2015 Accepted 1 March 2015

The application of the biocathode for hydrogen production in a Microbial Electrolysis Cell (MEC) is a promising alternative to precious metal catalysts. However, biocathodes are still in the improvement and development stages and require a deep understanding of the bioelectrochemical mechanisms involved. In this review, the results of biocathode MEC experiments and studies in the literature on biocathode development methods were summarised; furthermore, used carbon sources and substrates in biocathodic compartments and microbial communities on the biocathode were characterised. Based on the respective articles that were examined, biocathode MEC may be developed and initiated in one of three categories: (I) half biological two-chambered biocathode MEC; (II) full biological two-chambered biocathode MEC; (III) full biological single-chambered biocathode MEC. In addition, various mixed cultures capable of producing hydrogen were identified, and predominant species were detected. Desulfovibrio paquesii, Desulfovibrio G11 and Geobacter sulfurreducens were also successfully tested as pure cultures in biocathode MECs. Further studies are necessary for an acute and experimental comprehension of the transfer of electrons and the energy conservation mechanism involved in the biocathode MEC, which may provide a cost-effective and practical implementation of this technology. & 2015 Elsevier Ltd. All rights reserved.

Keywords: MEC Biocathode Hydrogen production

Contents 1.

2.

3.

n

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. MFC to MEC development. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2. MEC and biocathode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biocathode MEC configuration and start-up process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Half biological two-chambered biocathode MEC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Full biological two-chambered biocathode MEC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Half biological two-chambered biocathode MEC and full biological single-chambered biocathode MEC comparative research . . . . . . . . 2.4. Challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Carbon sources in biocathode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Studied substrates regarding hydrogen production application in biocathode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Studied substrate for wastewater application in biocathode . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Corresponding author. Tel.: þ 60 389118588; fax: þ 60 389118530. E-mail addresses: [email protected], [email protected] (M. Ghasemi).

http://dx.doi.org/10.1016/j.rser.2015.03.003 1364-0321/& 2015 Elsevier Ltd. All rights reserved.

24 24 24 25 25 26 26 26 27 28 29

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T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

4.

Biocathode microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Mixed cultures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Pure cultures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5. Future work . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

29 29 31 31 32 32 32

1. Introduction similar oxidation half reaction (Eq. (3)) [14] Growing global energy demands are an inevitable issue due to the high rate of population increase and fast industrial development. Currently, the major portion of energy demand is provided with conventional fossil fuel sources. Depletion and environmental pollution are two main problems associated with non-renewable fossil fuel sources; therefore, current research is more motivated towards locating renewable and clean sources of energy [1,2]. In this regard, bioelectrochemical systems (BESs) have significant potential for generating power, along with simultaneous wastewater treatment [3–5]. Living cultures, as the environmental friendly biocatalysts, displayed a sustainable role in bioenergy application [6]. Among the discovered BESs, Microbial Fuel Cells (MFCs) and microbial electrolysis cells (MECs) have attracted increased attention due to their ability to produce bioelectricity and biohydrogen, respectively [7].

1.1. MFC to MEC development It was in the late 18th century that the first empirical evidence of energy production in the form of bioelectricity was approved by Luigi Galvani via connection of frog legs to a metallic conductor. However, the first MFC was fabricated by Potter in 1911 upon the illustration of spontaneous current flow between an anode and a cathode electrode applied in a bacterial culture (bioanode) and sterile medium (abiotic cathode), respectively [8]. Promising sustainable energy production along with wastewater treatment attracted increased scientific attention towards this technological development, significantly during recent decades [9]. It was discovered that the current generation reported by Potter was due to decreased redox potential during bacterial growth. Kim et al. innovated the present MFCs which employed electrochemically active bacteria, and were able to use the electrode as the electron acceptor/sink in 1999; achieving the first enrichment of microbial community to generate electricity in the MFC basis electrochemical cell in 2004 [10,11]. Bioelectrochemical degradation of substrate (e.g. acetate) by living microorganisms released protons and carbon dioxide into anolyte and electrons to the anode as an oxidation half reaction in a typical two-chambered MFC (Eq. (1)) [12] C2 H3 O2  þ 2H2 O-2CO2 þ8e  þ7H þ ;

E1acetate=CO2 ¼  0:289 V vs:NHE at pH ¼ 7

ð1Þ

Electrons flow through an external circuit to the counter (cathode) electrode to produce bioelectrical current. Protons diffuse across the separating membrane to the cathode where they combine with electrons to form water in the presence of a final electron accepter (e.g. oxygen) as the reduction half reaction and complete the circuit (Eq. (2)) [12,13] O2 þ4H þ þ 4e  -2H2 O; E1H þ =H2 O ¼ þ 0:818 V vs:NHE at pH ¼ 7

ð2Þ

In the absence of oxygen, H þ ions may be supported with an extra applied voltage to be reduced to H2 in a modified MFC with

H þ þ 2e  -H2 ; EH þ =H2 ¼  0:412 Vvs:NHE

ð3Þ

Fig. 1 represented a schematic demonstration of MFC and MEC systems with the components involved.

1.2. MEC and biocathode The preliminary discovery of microbial hydrogen production in a MFC basis reactor, named the Microbial electrolysis cell (MEC), was reported by some researchers in 2005 (the so called technology was microbial electrolysis cell) [15,16]. From an economic perspective, it is believed that MECs are more environmentally beneficial due to their functionality for producing chemical products (notably H2) when compared to MFCs with present insufficient power outputs [17]. Microbial electrolysis cells provide energy required for H þ to H2 reduction (  0.412 V) via a microbial electrical supply ( 0.289 V), along with an external applied voltage. The extra applied voltage is around 0.14 V theoretically, and more than 0.2 V in practice when considering electrodes’ overpotentials and ohmic losses; however, it is still significantly lower than what is needed for water electrolysis (2.3 V) [18]. In addition, COD yields are considerably higher in MECs (60–100%) compared to conventional hydrogen production methods; e.g. steam reforming (63%), methanol cracking (45%) and water electrolysis (19%). On the other hand, hydrogen and carbon dioxide can be produced separately by microbial electrolysis systems in contrast with phototrophic fermentation which requires a two-stage process to produce a mixture of these two gas products [19]. Expensive metal catalysts, such as platinum, are commonly applied as the electrode catalyst to reduce overpotentials in MECs and MFCs. Platinum had formerly displayed promising results in conventional electrochemical systems due to its low activation overpotential. In addition to cost, platinum is non-renewable, scarce, subject to be poisoned by CO and sulphur and holds negative effects on the environment [20]. The cathode plays an important role in MEC systems where hydrogen is produced. The cathode and its loaded metal catalyst contribute around 47% of the total costs in MFCs [21]. The set up cost is a considerable, prevalent and challenging factor (concern) for researchers in the field of bioelectrochemical systems which will require a solution so as to deliver these new technologies into a heightened level; out of the labs [22]. Proposed drawbacks related to applying metal catalysts prompted current studies to focus more on cost effective catalysts [7,23–27]. Favourably, from among others, microorganisms have a special rate of interest that made them an inexpensive alternative since they are environmentally friendly, hold a self-generative character and are resistant to certain levels of impurities such as sulphur [28]. In a biocathode MEC, microorganisms are able to use the surface of the electrode as an electron source to catalyse the reaction of electrons and protons to form hydrogen.

T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

e-

E vs. NHE(mV)

e-

V

CO2

25

O2

+818 O2 /H 2 O Out

H2O

H

CO2

H2O

H

Feed In

H

Acetate

Anode

O

Cathode

0

Membrane

e

PS

CO

Out

H

-289 Acetate/CO 2 H

- 414 H+/H 2

H Feed In

H

Acetate

Anode

0

e

H

CO

Spontaneous v oltage generating reaction in MFC

O

Nonspontaneous power -source required reaction in MEC

H

Cathode

Membrane

Anode Cathode

Fig. 1. Schematic overviews of MFC and MEC by demonstration of standard potentials (vs. NHE) of oxidation and reduction reactions in anodic and cathodic chambers, resulting in a spontaneous reaction in MFC and a nonspontaneous reaction in MEC.

Improving the functionality of the biocathode as a promising alternative to precious metal catalysts in terms of overpotential, hydrogen production yield, start-up time and cathodic hydrogen recovery may lead this new encouraging technology into an industrial scale by focusing on hydrogen production from a wide range of renewable sources with low capital cost. This paper reviewed the biocathode development procedures, biocathodic nutrient sources, as well as, microbial communities that were applied by different scientists in published biocathode MEC research articles thus far.

Fig. 2. Different start-up methods of MEC biocathode using one or two-chamber reactors. Category I: half biological two-chambered biocathode MEC. Category II: full biological two-chambered biocathode MEC. Category III: full biological single-chambered biocathode MEC.

2.1. Half biological two-chambered biocathode MEC 2. Biocathode MEC configuration and start-up process Similar to the configuration of MFCs, MECs consist of an anode, a cathode and an optional separating membrane [29]. Employing the membrane is preferred due to the advantage of producing CO2 and H2 gases separately in the anodic and cathodic chambers, respectively. In addition, there is no propitious condition for methanogens to consume H2 gases in the presence of the membrane in an abiotic cathode MEC. Additionally, a power source is essential to supply energy required for non-spontaneous reactions (hydrogen production) in MECs in contrast to spontaneous reactions (water formation) in MFCs (Fig. 1). A few start-up procedures were applied by various researchers to initiate a biocathode MEC, the most common of which were mentioned in this paper. The first procedure involved a full biological start-up with electrochemically active microorganisms in both compartments of a twochambered MEC and/or in a membraneless one-chambered MEC. The second procedure consisted of a half (cell) biological start-up by applying the electrode polarity reversal to change a bioanode to the biocathode and/or transferring the active culture, or bioelectrode, of another MEC to the cathode chamber without polarity reversal; both with an abiotic anode. In other words, there are three categories of biocathode MEC based on the start-up and development process reported in the biocathode MEC literature so far: (I) half biological two-chambered biocathode MEC; (II) full biological two-chambered biocathode MEC; (III) full biological single-chambered biocathode MEC (Fig. 2).

The first microbial-origin biocathode MEC was established through a three step start-up procedure in a two-chambered bioreactor (Category I, Fig. 3i): (a) enriching an acetate-fed bioanode with electrochemically active mixed culture, accompanied by flushing the headspace with H2; (b) replacing the acetate with sodium bicarbonate and persistent hydrogen flushing; and (c) reversing the polarity of the electrodes accordingly (Fig. 3ii). Microorganisms were allowed to grow in the first 50-h batch mode to prevent the wash-out phenomena before switching to the continuous flow of the nutrient medium. Around 250 h after inoculation, the biocathode MEC was achieved by performing a polarity reversal scan in advance. The biocathode reached to 1.1 A/m2 of current density at  0.7 V potential, which was 2.4 times the current density obtained in another study by titanium electrode coated with platinum [30]. Promising results were shown by comparing the potential applied for the same value of the current density ( 0.47 A/m2) for platinum coated (with  0.7 V) and biocathode (with  0.65 V) MECs. Hydrogen yield tests demonstrated 0.63 m3 H2/m3/day which was subjected to 67–94% of hydrogen loss, mostly due to hydrogen diffusion through the membrane. Carbon limiting was applied to halt hydrogen consumption by methanogens upon removing bicarbonate from the nutrients before hydrogen tests. Pisciotta et al. [31] applied a novel method to develop a biocathode originating from the bioanode of a sediment microbial fuel cell without the need for set potentials or chemicals, such as ferricyanide, used in earlier bioanode to biocathode inversed study. The choice of sediment MFC was to provide an anaerobic condition comparable to typical

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T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

Fig. 3. (i) Schematic of the first biocathode MEC experimental set up. “Reprinted with permission, Copyright (2014) American Chemical Society”; (ii) Three-step biocathode development procedure in the first half biological biocathode MEC: (a) enriching an acetate-fed bioanode with electrochemically active mixed culture accompanied by flushing the headspace with H2, (b) replacing the acetate with sodium bicarbonate and persistent hydrogen flushing, (c) reversing the polarity of the electrodes accordingly. Ferocyanide/ferricyanide was used as an electron donor and acceptor. “Reprinted with permission, Copyright (2014) American Chemical Society” [25].

electrode suspension in the electrolyte that was more susceptible to dissolved oxygen contamination through gaskets and seals, or media replacements [31]. Table 1 displayed the experimental conditions and obtained results of various biocathode MECs reported in the literature so far. 2.2. Full biological two-chambered biocathode MEC Although the first half cell biological biocathode MEC research approved the application of microorganisms as the cathode catalyst, it still functioned under half biological conditions (bioanode and abiotic cathode in the first two steps, and biocathode and abiotic anode after polarity reversal in the third step). Jeremiasse et al. [41] studied the first full biological electrolysis cell in which both oxidation and reduction reactions were biocatalysed with electrochemically active microorganisms (bio-cathode and anode) in the same experimental setup as in [25] (Category II). The biocathode was inoculated 600 h after the establishment of the bioanode from previous polarity reversed experimental setups [25]. Current density of 3.3 A/m2 was obtained at the cathode potential of  0.7 V (applied voltage of 0.8 V) which was comparable with that of a continuous membraneless MEC of 3.2 A/m2 catalysed with 5 g/m2 load of platinum [42]. However, the result was far from the current density of 11.7 A/m2 in another membraneless MEC operated in the batch mode and coated with 5 g/m2 load of platinum [43]. Low hydrogen rate of 0.04 N m3/m3/day and cathodic hydrogen recovery of 21% were reported despite applying a carbon limiting condition, which were lower than those obtained in the same experimental setup for the first half biological biocathode MEC (0.63 m3 H2/Volume/day and 49%, respectively) [25] (Table 1). 2.3. Half biological two-chambered biocathode MEC and full biological single-chambered biocathode MEC comparative research As a comparable study, biocathode MEC was investigated in an inverted bioanode half cell (Category I) after substrate depletion and was compared to an identical membraneless MEC (Category III) in the same study that operated with applied voltage from the start (Fig. 4i). The highest hydrogen production rate of about 24 mmol/h was reported at a cathode potential of 1.0 V with 56% cathodic hydrogen recovery in the biocathode MEC, and with ferricyanide in the anode. The results for membraneless MEC at a similar cathode potential of 1.0 V (0.7 V applied voltage) were 10.8 mmol/h of hydrogen production rate and 36% of cathodic hydrogen recovery. However, it was unclear whether any biocatalytic (biocathode) activity by microorganisms in one compartment of MEC was present in this research [15]. Fu et al. [37] investigated

the biocatalytic activity of the cathode by developing one and twochambered biocathode MEC without polarity reversal (Categories III and I, respectively; Fig. 4ii). It was the first alternative method for developing a biocathode without reversing the polarity of the electrodes. First, the biocathode was developed in a membraneless MEC by inoculating from a three months advanced in operation MFC, and then investigated for biocatalytic activity of the electrodes (Category III). Afterwards, the cathode of the membraneless setup was placed as the biocathode of the two-chambered MEC (“C-C”). In addition, the anode of the membraneless setup was also placed as the biocathode (“A-C”) to compare results with those from polarity inverted bioanodes to biocathodes (category I). The abiotic anode with oxidation of potassium ferrocyanide was applied. Cyclic voltammetry proved catalytic ability of the anode for acetate oxidation, and higher catalytic activity of the cathode to produce H2 in comparison to the anode in the single-chambered experiments. By performing further analysis in the twochambered setup, large cathodic currents were obtained at the potential of 0.65 V in C-C design compared to small amounts recorded in the A-C design at the potential of less than 0.7 V [37]. Similar to previous comparable studies [15], lower cathodic H2 recovery was obtained for the membraneless setup (20%) compared to the two-chambered biocathode MEC (70%). At cathode potential of  0.8 V, current density of  1.28 A/m2 and hydrogen production rate of 376.5 mmol/day/m2 were recorded for the C-C configuration (Table 1).

2.4. Challenges Hydrogen lost across the membrane was a considerable fact that maintained both membraneless and two-chambered configuration and were attractive research subjects. Although using a membrane in an abiotic cathode MEC was preferred due to the prevention of methanogens to consume H2 in the product chamber, the membrane had other aspects that required study. Although, there was the potential of methanogenisis in biocathode MEC, nonetheless. Furthermore, applying the membrane presented high hydrogen loss and scaling problems; however, membraneless setups resulted in low cathodic H2 recovery which was probably due to the utilisation of H2 products by exoelectrogens to produce electricity on the anode. On the other hand, full and half biological biocathode had their own issues that were not yet addressed or completely studied. Scaling and bioanodic associated limitations were prevented in the full biological two-chambered biocathode setup, while the two-chambered was able to produce higher current density. A profound understanding of

T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

27

Table 1 Overview of experimental conditions and obtained results for various biocathode MECs reported in the literature. Biocathode start-up process

Biocathode type

Biocathode catalyst

Membrane Cathodic chamber size (ml)

Mode of operation

Cathode potential (V)

Hydrogen production rate (m3 H2/ m3 reactor/ day)

Hydrogen recovery (%)

Current (A/m2)

Ref.

Category Ia

Graphite felt, S.Ab ¼250 cm2, Thc ¼ 6.5 mm Non-porous flat graphite in contact with graphite felt filled in chamber S.A¼ 22 cm2 Graphite felt, Th¼ 6 m Graphite felt, Th¼ 2.5 m Graphite rod S.A¼ 9.7 cm2 D¼ 6 mm Brush Graphite fibre S.A ¼0.22 m2 Graphite granules 30 g (dry weight)

Active mixed culture taken from an active bioelectrochemical cell

CSMd

250

Continuous, 1.3 ml/min

 0.7

0.63

49

 1.2

[25]

Pure culture of G. sulfureducens filtered and re-suspended in biocathodic cell

CEMe

33

Continuous, 0.85 l/h

1

0.43 (24 mmol/h)

56

 2.4

[32]

Graphite granules 30 g (dry weight) Plain carbon cloth S.A¼ 40 cm2

Graphite paper, S.A¼ 22 cm2 Graphite felt, S.A¼ 100 cm2, Th¼ 0.25 cm Filled with granular graphite along with graphite electrode S.A¼ 0.052 cm2 Graphite felt S.A¼ 100 cm2

Category IIa

Carbon paper S.A¼ 8 cm2 Graphite felt, S.A¼ 250 cm2, Th¼ 6.5 mm

Active culture taken from a four-year CSM culture enriched in MFC and MEC Pure Culture of Desulfovibrio G11 CEM

250

Continuous

 0.7

0.63

–

1.2

[33]

250

 0.7

–

–

0.76

[33

Pure culture of Desulfovibrio paquessi PEMf

270

Continuous 60 ml/min Batch

 0.9

0.12

3

[34]

Transferred biocathode from a sediment MFC Brewery wastewater

CEM

190

Batch

 0.539

0.08 mmol

–

 0.45 mA [31]

PEM

150

Batch

 590

–

–

[35]

PEM

150

Semi batch

 590

0.295 (11.8 mM/ day) 2.5 (100 mM/ day) 376.5 mmol/ day/m2

2.5

–

[36]

70

 1.28

[37]

From previous electrosynthetic cell that originally was inoculated with brewery wastewater Transferred Biocathode from previous single chambered biocathode setup inoculated with mesophilic microorganisms. Effluent of a previous operated MEC

PEM

300

Batch

 0.8

CEM

33

 0.7

–

–

1

[38]

Effluent from a MEC biocathode

CEM

100

Continuous 36 ml/h Continuous 156 ml/h

 0.7

2.4

–

2.7

[38]

A mixed effluent of urban wastewater treatment plant and from a MFC used for treating waste

CEM

390

Continuous HRT¼ 6.25

 0.9

0.1

–

17A/m3

[39]

Effluent from a 30-day in run biocathodes, which were inoculated with a culture collected from UASB reactor and enriched in anodes of MECs over 5 years

CEM

–

Continuous 60 ml/min

 0.7

2.2

50

2.7

[28]

Dechlorinating cultures maintained in anaerobic reactors Effluent from the biocathode in Ref. [25]

PEM

270

Batch

 0.75

0.01

–

4.4

[40]

CSM

250

Continuous, 1.3 ml/min

 0.7

0.04

21

3.3

[41]

–

250

batch

 0.8

20

-0.87

[37]



33

Continuous

 1.13

0.46 mmol/ day/m2 0.31 (17.2 mmol/ h)

43

1.21

[32]

Category IIIa Plain carbon cloth Effluent from a thermophilic threeS.A¼ 40 cm2 month in operated MFC Graphite electrode Pure culture of G. sulfureducens filtered and re-suspended in biocathodic cell

a Category I: half biological two-chambered biocathode MEC; Category II: full biological two-chambered biocathode MEC; Category III: full biological single-chambered biocathode MEC. b S.A ¼surface area. c Th¼ Thickness. d Cation selective membrane. e Cation exchange membrane. f Proton exchange membrane.

the microorganisms involved in H2 formation and electron uptake mechanism in the biocathode may help to enhance the biocathode MEC in both one and two-chambered design; based on the application and condition. Table 2 summarised relevant issues relating to three mentioned categories discussed in published articles regarding biocathode MECs.

3. Carbon sources in biocathode Although bioelectrochemical systems (such as MECs) recorded lower product yields compared to chemical methods, they are still considered to be a promising technology due to their potential to use renewable resources and wastewater as a wide range of

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T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

Fig. 4. (i) Schematic of two-chambered MEC converted to a biocathode MEC for testing the ability of Geobacter sulfurreducens for hydrogen production in biocathode MECs. “Reprinted with permission. Copyright (2014) American Chemical Society” [32]; (ii) (A) single and (B) two-chambered MEC setups in which bioanode and biocathode of single chambered MEC were transferred to two-chambered as the biocathode in two separate experiments. “Reprinted with permission. Copyright (2014) International Journal of Hydrogen Energy (IJHE)” [37]. Table 2 The pros and cons reported for three categories of biocathode MEC, along with predicted discussed solutions and reasons. Category

Advantages

Reported problems

Cathodic and anodic reaction after biocathode development

Reasons

Suggested solutions

Category I

1. Low scaling effects 2. No possible limitation by a bioanode [28]

1. Consumption of hydrogen by hydrogenotrophic methanogens [25] 2. Low cathodic hydrogen recovery [25]

Anodic: ([Fe(CN)6]4  -[Fe(CN) 6]3  þ e  ) Cathodic: (CO2 þ H2O2H2CO32H þ þ HCO3 ) [37]

1. Hydrogen loss by diffusing through the membrane

1. Removing the carbon source from cathodic medium (carbon limiting policy) [25] 2. Using a thicker membrane, or other membrane materials 3. Providing higher current density that produce more hydrogen, while diffusional hydrogen loss are constant [25]

Category II

1. High current density [41]

1. Low hydrogen recovery [41] 2. Methane detection in biocathode chamber despite carbon limiting policy 3. Current density drop after long time of operation [41] 4. Hydrogen loss

–

1. Hydrogen loss is a result of H2 diffusing through the membrane and tubing 2. Methane may have been formed by methanogens present in the bioanode, and subsequently crossed via the membrane to the biocathode 3. Methane could have been formed by methanogens present in the biocathode from hydrogen and carbon dioxide (originating from the bioanode) 4. Precipitation of calcium phosphate on the biocathode

1. Higher current density, higher hydrogen recovery 2. More extensive research on the type of the membrane is required

Category III

1. No scaling, resistance and loss due to absence of membrane

2. Low cathodic H2 recovery [37] 3. Contamination of cathodic product with anodic gas product

–

1. H2 produced in the singlechambered MEC was oxidised by the exoelectrogens on the anode which led to electricity generation [37]

feedstock. In addition, BESs are cost effective and can reduce energy demands. From this aspect, biocathode MEC are appreciable since they are less susceptible to poisonous components present in real wastewaters or natural resources, in comparison to metal catalysts. To develop a biocathode MEC, a carbon source is necessary to supply cathodic biocatalyst growth; furthermore, they have shown effective impact on main/side product formation. The substrates used in different biocathodic electrolysis systems were reviewed by considering two discussed applications: hydrogen production and wastewater treatment.

3.1. Studied substrates regarding hydrogen production application in biocathode In the first biocathode MEC, sodium acetate was replaced by sodium bicarbonate before bioanode conversion to the biocathode. No hydrogen was detected and methane was the only product. By assuming that the bicarbonate served as a carbon source for hydrogenotrophic methanogens for consuming hydrogen, carbon limiting strategy was applied by removing the bicarbonate before hydrogen tests. Authors claimed that they preserved this strategy for

T. Jafary et al. / Renewable and Sustainable Energy Reviews 47 (2015) 23–33

more than 1000 h without effecting the current generation in the biocathode system [25]. However, the carbon limiting strategy was not efficient in the full biological two-chambered MEC, fed with sodium bicarbonate in the cathode medium and sodium acetate in the anode medium. It was reported that detected methane may have been produced in the bioanode and then diffused across the membrane to the cathode; or methanogens in the biocathode could have utilised CO2 of the anode and H2 of the cathode chambers to form methane [25,41]. In addition, a biocathode requires a long adaption and start-up time, along with low production rate, in comparison to metal catalysts. It was reported that the replacement of bicarbonate as an autotrophic, with acetate as a heterotrophiccarbon source, has improved the start-up procedure’s time duration to double; and further improved the H2 production rate to seven times, about 2.2 m3 H2/m3 reactor/day compared to previous studies [25,28]. This was the highest level of hydrogen production rate in the biocathode MEC so far. Additionally, the sulphate element was removed from the media to stop growth of sulphate reducing microorganisms in this research. No methane and hydrogen sulphide were detected. In a recent study, Jeremiasse et al. [38] had experimented with biocathode MECs to determine how carbon sources will affect the growth and microbial communities in the biocathode development process. Acetate, bicarbonate and acetate without sulphate-fed MECs were studied in five experimental setups. Although applying acetate as the carbon source displayed half the start-up time compared to bicarbonate (28 days to 63 days, respectively), insignificant results were obtained regarding the average current and H2 yield; irrespective of carbon source. Furthermore, it was concluded that the design had a considerable influence on the biocathode development and its biofilm composition [38]. In another biocathode study performed by Marshal et al., carbon dioxide presented a capability as the sole carbon to produce hydrogen at the rate of 11.8 mM/day at cathode potential of  590 mV; aside from acetate and methane as two other coproducts in an electrosynthetic system [35]. The results improved to around 100 mM/day at the same cathode potential of  590 mV in a similar experimental setup operated in a semi batch mode over 150 days in a later study [36]. Table 3 summarised the biocathode electrolysis experiments by considering the used carbon sources, and analysed microbial communities that may have been affected by carbon sources as one of the effective parameter. 3.2. Studied substrate for wastewater application in biocathode Wang et al. [44] investigated the toxic nitrobenzene wastewater (NB) conversion to a less poisonous product of aniline in a biocathode BES in the presence of glucose and bicarbonate at 0.5 V of applied voltage. While nitrobenzene reduction presented a 10% decrease by replacing glucose to bicarbonate, selective reduction of nitrobenzene to aniline at a high rate of 98.93% was nevertheless achieved. Nitrobenzene reduction in this biocathode system was considerable compared to earlier NB reduction studies in an abiotic cathode and MFC system with pt loaded cathode; in regards to the overpotential, precious metal catalyst application and chemical costs [8,45,46]. Hydrogen measurement was not the focus of this research; however, hydrogen was studied to see whether it can play an electron donating role for nitrobenzene reduction in the system. The research results suggested that the autotrophic condition may not be necessary and developing the biocathode was possible with glucose as an organic carbon source that is generally available in the real environment [44]. During a subsequent research in 2014, Liang et al. [47] increasingly studied the NB reduction to aniline by switching organic carbon source (glucose) to an inorganic source (bicarbonate) in a biocathode BES. They focused on: (a) the effect of carbon source exchange on

29

biocathode catalytic properties and (b) further investigation of microbial communities in biocathode biofilms as a result of carbon source switchover. Eight reactors were employed to handle experiments in fed batch modes; five were running under glucose with different concentrations, two were focusing on carbon source switchover experiments (glucose to bicarbonate), while the other was kept operating with the abiotic cathode for trustworthy comparison purposes. Four various modes were considered for the NB reduction process: mode—(a) glucose-fed biocathode; mode—(b) glucose-to-bicarbonate switchover to biocathode; mode—(c) open biocathode; mode—(d) abiotic cathode. NB nevertheless continued reducing to aniline after carbon source switchover, however, with a lower NB reduction and aniline formation rate [47]. The results were consistent with those reported in previous studies [44]. Authors had performed detailed research on the effect of carbon switchover regarding the biocathode microbial community which will be discussed later in this paper. Azo dye could also be successfully removed in a single-chambered biocathode electrolysis system at 0.5 V of applied voltage. Biocathode setup showed 81.7% of removal efficiency in just 10 h, which was around 13% higher than what was achieved in an abiotic cathode [48]. In another research study, a type of antibiotic-content wastewater was also treated in bio and abio-cathode electrolysis systems, and the cathodic reduction process was investigated (at 0.5 V of applied voltage). Higher current peaks, lower overpotential and less toxic intermediates were observed at the biocathode in comparison to those in the abiotic cathode. Glucose was used as a carbon source to donate electron intracellularly, while the electrode fulfilled an extracellular electron donation role (Table 3) [48].

4. Biocathode microorganisms When applying living cultures as the biocatalysts on the cathode, there are some basic requirements that microorganisms must satisfy in order to catalyse half reduction reactions. Biocatalysts should be capable of overcoming thermodynamic limitation to form hydrogen by externally applied voltage. In addition, the electrode surface should be utilised as an electron source (donor) by biocatalysts through the biocatalytic activity of pure or varied species of mixed cultures to reduce H þ ions to hydrogen, CH4 and other expected products [32,49]. Rosenbaum et al. extensively reviewed the possible Extracellular Electron Transfer (EET) mechanisms through published articles on the biocathode, as well as, known mechanisms for biological processes. Finally, they suggested that c-type cytochrome, along with hydrogenases, would be engaged in bioelectrochemical processes for direct electron transfer [50]. Hydrogenases are the enzymes involved in bioelectrochemical systems to catalyse H2 production/consumption [51–53]. There are three categories for hydrogenases based on their metal sites that are active for a reduction reaction: nickel–iron, iron– iron and iron–hydrogenases (Ni–F, Fe–Fe and Fe–hydrogenases, respectively) [54,55]. However, using purified hydrogenases include the related drawback of low stability and catalytic activity during long durations, which can be improved by using whole cells [33]. MECs suffer from a lack of knowledge regarding the biocatalytic hydrogen formation mechanism, the type of involved hydrogenases in H2 evolution, active microorganism on the biocathode, electron uptake mechanism from the bioelectrode and energy management by the cell. 4.1. Mixed cultures The first mediatorless biocathode MEC was developed by using natural mixed culture with microbial origin. The microbial originality of the microorganisms was investigated by the inhibition test (by exposing the biocathode to carbon monoxide), along with subsequent inoculation to a new biocathode setup; however,

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Table 3 Summary of the dominant microorganisms identified in biocathodic electrolysis cells. Hydrogen revealed cathode potential

Dominant species

Carbon source

Biocathode development procedure

Detected Products

Analysis used for Ref. biofilm characterisation/ study

Brewery wastewater

 590

CO2

Biocathode origina

Methane, acetate and hydrogen

Marine sediments

o  400

Acetobacterium spp, Sphingobacterials, Methanobacterium (Firmicutes, Bacteroidetes, Proteobacteria, Deferribacteres, Synergistetes and Spirochaetes at phylum level) Autotrophic: Eubacterium limosum, Desulfovibrio sp.A2, Rhodococcus, Gemmata obscuriglobus

Bioanode of the sediment MFC

Methane, hydrogen

Dechlorinating bacteria

 450 (with redox mediator),  700 (without redox mediator) o  900

No added organic carbon after biocathode start-up No organic carbon source

Biocathode origin

Hydrogen

[35] CV, RNA extraction, RTPCR amplification, 16S rRNA sequencing, SEM [31] LSV, DNA extraction and 16S rRNA gene amplification, Gram staining Eubacterial probe [40]

Culture source

Mixed culture

A mixed affluent of urban wastewater treatment plant and from a MFC used for treating waste

Pure culture

a b

Desulfitobacterium spp., dehalococcoides spp.

Hoeflea sp., Aquiflexum sp.

Bicarbonate

Biocathode origin

Hydrogen

Activated sludge

 0.74

Enterococcus sp. (Firmicutes at phylum level)

Glucose & bicarbonate

Biocathode origin

Hydrogen, aniline

Microbial origin mixed culture

 0.7

Rhodopseudomonas palustris (Proteobacteria at phylum level)

Bicarbonate

Reversed bioanode

Hydrogen

Activated sludge

–

Enterococcus (Firmicutes at phylum level) Paracoccus & Variovorax (proteobacteria at phylum level) Firmicutes phylum

Glucose

Biocathode origin

Aniline

Biocathode of a single-chambered setup placed as the biocathode of the dual-chambered setup Biocathode origin

Hydrogen

Thermophilic microorganism from a previous MFC setup

 0.7

Effluent of a previous operated MEC

 0.7

Effluent of a previous operated MEC and MFC

 0.7

Pure culture of G. Sulfurreducens

 0.8

–

Pure culture of Desulfovibrio paquesii Pure culture of Desulfovibrio G11

 900

 700

Bicarbonate No added carbon source after biocathode start-up

Acetate, Clostridium cylindrosporum, bicarbonate Desulfotomaculum sp., Clostridium cylindrosporum, Desulfotomaculum sp. Hydrogenophaga flava, Azonexus caeni (At phylum level: Firmicutes for small setups and proteobacteria and bacteroidetes for large setups, regardless of carbon source) Desulfovibrio vulgaris (protebacteria Bicarbonate at phylum level), Desulfitobacterium hafniense (Firmicutes at phylum level) Rikenella microfusus (Bacteroidetes at phylum level)

DNA extraction and 16S rRNA gene amplification, SEM, DNA extraction DNA extraction and 16S rRNA gene amplification DNA extraction and 16S rRNA gene amplification Gene array, DNA extraction and 16S rRNA gene amplification, CV DNA extraction and 16S rRNA gene amplification, CV

[39]

[44]

[49]

[47]

[37]

Hydrogen

SEM, DNA extraction and 16S rRNA gene amplification, DNA microarray analysis

[38]

Bioanode inversed biocathode

Hydrogen

DNA extraction and 16S rRNA gene amplification, clone library analysis, DGGEb

[33]

Bioanode inversed biocathode

Hydrogen

–

[32]

–

No added carbon source after biocathode start-up Bicarbonate

Biocathode origin

Hydrogen

–

[34]

–

Bicarbonate

Biocathode origin

Hydrogen

–

[33]

Biocathode was developed by culturing the cathode directly with microorganisms in the cathodic compartment from the beginning. Denaturing gradient gel electrophoresis.

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microbial active species and mechanism were not analysed and studied [25]. Following the proof-of-principal of a full biological two-chambered MEC by Jeresmiasse et al. [41], microbial diversity of the bioanode and biocathode was scrutinised in a MEC developed with similar start-up procedures as Rozedal et al. [25] and Jeresmiasse et al. [41]; it was inoculated with a mixed culture [49]. Two clones associated with Bacteroidetes and Firmicutes phyla were identified in the bioanode which were previously reported in anodes of various MFCs [56,57]. Rhodopseudomonas palustris was assessed as the dominant species in the cathodic bioelectrode which had Ni–Fe and Fe–Fe–hydrogenases, and was a known species in hydrogen production processes [57–60]. In an extensive experimental research, Croese et al. [38] characterised the bacterial diversities of five biocathode MECs that were different in size, electrode material, flow path and carbon source. Firmicutes in small MECs, and proteobacteria and Bacteroidetes in large MECs, were classified as prevalent groups in both acetate and bicarbonate fed MECs but with various percentages. Actinobacteria by 98% was revealed as the dominant associated group in the large MEC fed with acetate by excluding sulphate from the media. Regardless of the carbon sources used in small setups, Clostridiaceae and Peptococcaceae were identified as the dominant ribotypes. Bacteroidetes and Betaproteobacteria were the prevalent ribotypes for acetate and bicarbonate large fed MECs, respectively. The differences between dominant species in large setups were more elaborately investigated by hydrogenases chips in this research. Ni–Fe and Fe–Fe hydrogenases and reducing hydrogenases coenzyme F420 were abundantly located in acetate fed biocathode MEC. Various Ni–Fe hydrogenases were the ample genes in bicarbonate-fed setups. Detailed information on dominant ribotypes, established hydrogenase gens and various phyla distributions were reported for all 5 experimental setups in this research article. Nevertheless, the effect of acetate or bicarbonate-fed MECs in this research study remained unclear, while no exclusive heterotrophic/autotrophic in respect to bacteria were distinguished [38]. However, glucose and bicarbonate feedstock resulted in two different heterotrophic and autotrophic dominant species in other biocathode electrolysis setups of nitrobenzene reduction research. Enterococcus in glucose-fed and Paracoccus and Variovorax in bicarbonate-fed biocathode systems were identified as the dominant species [47]. Substantial performance achieved by thermophilic microorganisms in some MFCs setups [61–64] provided the idea for the first MEC biocathode which was developed with thermophilic microorganisms in 2013 [37]. Analysing thermophilic biocathode microbial community revealed 21 phylotypes which belonged to six phyla; dominated by the Firmicutes phylum. Hydrogenophilic dechlorinating cultures (desulfitobacterium and dehalococcoides-enriched cultures) may also catalyse H2 production in biocathode MECs with methyl viologen at the cathode potential of  450 mV, and without mediator at potentials less than  700 mV [40]. 4.2. Pure cultures Other than mixed cultures, Geobacter sulfurreducens and Desulfovibrio species were investigated in some research studies for their ability to catalyse H2 formation from polarised graphite electrodes and their ample information on electron uptake mechanisms. G. sulfurreducens is a well-known biocatalyst that was tested in both anode and cathode of MFCs, and also as a biocatalyst in the MEC anode. From its four encoded hydrogenases, two are believed to be in the cytoplasm and two others are membrane-bound hydrogenases involved in hydrogen uptake by this biocatalyst. Both bioanode inversed biocathode of a two-chambered MEC and biocathode origin of a single-chambered MEC inoculated with this biocatalyst displayed a considerable level of hydrogen production at the cathode

31

potential of less than  0.9 V [32]. As previously mentioned in this section, energy-conserving hydrogenases, or cytoplasmic hydrogenases coupled with membrane-bound ATPase, are believed to be energy conservation-associated mechanisms for hydrogen production in biocathodes. G. sulfurreducens illustrated the presence of two cytoplasmic hydrogenases, yet no possession of energy-conserving hydrogenases were recorded by this genome [59,65]. Geelhoed et al. reported that the proton gradient resulted by these hydrogenases through the cytoplasmic membrane could be controlled by a membrane-bound ATPase [32]. Furthermore, the cell attachment process on the anode and the cathode of the single-chambered setup also required additional study. It was assumed that the cell may detach after growth on the bioanode and initiate its function on the cathode. Desulfovibrio species are known microorganisms for their ability to catalyse hydrogen production reaction [58,66]. Attached Desulfovibrio. paquesii to the graphite biocathode could successfully catalyse hydrogen generation at the cathode potential of less than  900 mV with 100% columbic efficiency [34]. Croese et al. investigated the microbial community in a biocathode MEC inoculated with a mixed culture. Proteobacteria and Firmicutes phyla were identified as the dominant bacterial population, and Desulfovibrio vulgaris as the dominant species. Subsequently, the application of Desulfovibrio G11 as the pure culture of biocathode MEC was investigated at the outset in the same study, without any mediator, at cathode potential of 0.7 V [33]. Calculating the energy available at the cathode by considering the cathode potential ( 0.7 V) required energy for hydrogen production ( 0.41 V) and overpotential concentration since cathode loss displayed enough available energy for microorganism growth. While some researchers now recognise the dominant species in biocathode MEC, further studies are required regarding biocathodes developed with pure cultures of dominant species in order to examine the involved genes in reduction half reactions. In addition, increased deliberation on the growth rate and yield, as well as, energy conservation and EET mechanism for biocathodic reaction are further necessary. An overview of the bacterial communities characterised in various biocatalysed cathode systems, along with the carbon source, detected products and respective analysis methods were collectively tabulated in Table 3.

5. Future work Biocathode MEC is a new technology that could play a significant role in leading recent attempts towards the delivery of bioeletrochemical systems out of the lab scale and into practical implementation by the replacement of precious metal catalysts. In this way, fundamental studies are necessary to characterise effective parameters, individually and integrally, to improve process yield in the form of energy and product. Additional research is mandatory to improve the performance of biocathode in MECs with respect to the hydrogen production rate and required applied voltage, which is still in turn, lower and higher than those achieved by metal-based cathodes [26,67–69]. Comprehensive studies are required to focus on the investigation and enrichment procedures of bacterial communities as the main catalysts in the cathode chamber to improve hydrogen formation. Although mixed cultures may consume a wider range of sources and are easier for maintenance, fundamental research on identified species of mixed cultures capable of providing hydrogen is still necessary to clarify the electron uptake mechanism. In spite of the many discussions on assumptions and hypotheses regarding the theoretical electron uptake mechanism from the cathode, a lack of experimental research is quite apparent in this area. Furthermore, a more comprehensive understanding of the reaction mechanism involved in the biocathode will aid in energy management, whether used by the biocathode for product formation

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purposes or consumed by microorganisms for growth. The link of hydrogen production to energy conservation and biocatalyst growth remains unclear. The electron transfer mechanism that uses the cathode as the electron donor, also needs to be understood as well. Further investigation is also necessary on the energy conservation in the biocathode of the MEC alongside studies on growth rate, yield and kinetic [32,33,50].

6. Conclusion Efficient hydrogen production in the biocathode MEC is a promising goal that can assist this novel technology to overwhelm the aspects of cost associated to current chemical catalyst sources application. The highest hydrogen production of 2.2 m3 H2/m3/day was achieved in a half biological two-chambered MEC with acetate and mixed microbial community in comparison to the first established biocathode MEC with 0.63 m3 H2/m3/day. Desulfovibrio species are recognised among detected gens in enriched mixed microbial communities capable of producing hydrogen when attached to an electrode surface. While the half biological setup displayed higher cathodic recovery and hydrogen product, it is nevertheless susceptible to high hydrogen loss across the membrane. On the other hand, it was reported that hydrogen loss across the membrane may be less important when high current density flows through the circuit. Although full biological twochambered setup may produce high current density, it nevertheless suffers from other problems such as the precipitation of electrodes and side product formation. Single-chambered MEC does not suffer from problems of resistance, scaling and product loss associated with existing membrane. However, it still suffers from very low product yield and contamination. Furthermore, the reactor design such as size and cathodic flow pattern had also demonstrated considerable effects on the microbial community of the biocathode biofilm which is one of the most interesting and unknown aspect of the field. Biocatalyst type, enrichment process and nutrient medium are other factors that affect the product evolution yield. Using acetate as the carbon source in the biocathode chamber resulted in the highest hydrogen production rate and had significantly decreased the start-up time. However, methane detection still led some researchers to use bicarbonate and carbon limiting strategies to overcome the methanogenesis growth. The long start-up duration could be overcome by using acetate as the carbon source to produce pure hydrogen product, in spite of the reported carbon limiting strategy due to methane detection. Energy management and the associated mechanism with electron–electrode–hydrogen evolution are still under investigation by scientists. Experimental discovery on the electron transfer mechanisms may further assist the enhancement in the present low hydrogen rate and cathode hydrogen recovery of biocatalysed cathode MECs, in comparison to metal based cathode MECs.

Acknowledgment The authors gratefully acknowledge support given for this work by 03-01-02-SF0985 Sciencefund from Malaysian Ministry of Science, Technology & Innovation, DIP-2012-27 from Dana Impak Penebitan from Universiti Kebangsaan Malaysia and ERGS/1/2012/ TK05/UKM/01/2 Exploratory Research Grant Scheme from Malaysian Ministry of Education. The author would like to thank Hexagon Synergy (M) Sdn Bhd for the support as well. References [1] Ghasemi M, Daud WRW, Hassan SH, Oh S-E, Ismail M, Rahimnejad M, et al. Nano-structured carbon as electrode material in microbial fuel cells: a comprehensive review. J Alloys Compd 2013;580:245–55.

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