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Process Safety and Environmental Protection 125 (2019) 83–91

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Process Safety and Environmental Protection


journal homepage: www.elsevier.com/locate/psep

Characterization of electricity production and microbial community


of food waste-fed microbial fuel cells
Bahareh Asefi a,b , Shiue-Lin Li c , Henry A. Moreno a,d , Viviana Sanchez-Torres a,d , Anyi Hu a ,
Jiangwei Li a,b , Chang-Ping Yu a,c,∗
a
CAS Key Laboratory of Urban Pollutant Conversion, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China
b
University of Chinese Academy of Sciences, Beijing, 100049, China
c
Graduate Institute of Environmental Engineering, National Taiwan University, Taipei, 106, Taiwan
d
Escuela de Ingeniería Química, Universidad Industrial de Santander, Bucaramanga, Colombia

a r t i c l e i n f o a b s t r a c t

Article history: Food waste (FW) contributes to a great proportion in the municipal solid waste and is generated during
Received 7 November 2018 disposal from different life cycles of food processing and consumption. FW treatment is a big challenge
Received in revised form 9 March 2019 and there is an urgent need to develop a suitable treatment technology. The microbial fuel cell (MFC)
Accepted 11 March 2019
is a promising bioelectrochemical technology using bacteria as the catalyst, which has been developed
Available online 12 March 2019
to effectively generate bioelectricity from diverse organic wastes. The present study investigated the
treatment of food waste collected from a Chinese canteen using MFCs under different conditions. It was
Keywords:
observed that the highest closed circuit voltage and maximum power density obtained were 775 ± 21 mV
Food waste
Microbial fuel cell
and 422 mW m−2 , respectively, when using food waste with nutrient medium as the anolyte and per-
Permanganate manganate as the catholyte. Under this condition, biodegradation processes in the MFCs could achieve
Ferricyanide 69 ± 18% COD, 88 ± 5% carbohydrate, 76 ± 9% protein, 65 ± 8% TOC and 71 ± 8% total nitrogen removal.
Microbial community Microbial community analysis using 16S rRNA gene high-throughput sequencing showed Firmicutes,
Power management system Bacteroidetes and Proteobacteria were the dominant phyla and Geobacter was the most abundant genus.
Therefore, our microbial community results suggested that the mixture of exoelectrogenic and fermenta-
tive bacteria have a pronounced effect on MFCs system treating FW while affecting on organic degradation
and energy production. A power management system was used to demonstrate that electricity from FW-
fed MFCs can be successfully harvested to provide intermittent electricity to loads. Overall, this study
demonstrated the potential of using MFCs for food waste treatment to achieve electricity production and
waste reduction.
© 2019 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.

1. Introduction FW ends up in landfill which is potentially responsible for increas-


ing greenhouse gases and global warming. Since FW brings a huge
Food waste (FW) in the municipal solid waste could be uti- challenge in developing countries like China (60 Mt FW per year)
lized for many applications including composting, fertilizer and (Li et al., 2017b), there is an urgent need to find suitable treatment
renewable energy recovery. FW is generated during disposal from technology to solve this problem. The major composition of FW has
different processes such as farming, post-harvest and packing, pro- been reported to contain 300–600 mg g−1 starch, 60–100 mg g−1
cessing, distribution, retail, food service and household usages. proteins and 70–300 mg g-1 lipids (Leung et al., 2012). Therefore,
According to the European Commission (Thi et al., 2015), FW could FW has high amount of organic waste with high energy content,
be divided into three categories which include: (1) food lost during and this characteristic of FW gives us opportunities to use FW in
production, (2) unavoidable wastes, like banana peels or fruit cores, many biotechnological processes for energy production (Pleissner
and (3) food to be eaten which is lost during consumption. Most et al., 2013).
The microbial fuel cell (MFC) is a promising bioelectrochemical
device using bacteria as the catalysts, which has been developed
∗ Corresponding author at: CAS Key Laboratory of Urban Pollutant Conversion, to effectively generate bioelectricity from diverse organic wastes
Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, (Mohd Yusoff et al., 2013; Nastro et al., 2017; Zuo et al., 2006).
China. In MFCs, the substrate would be oxidized by active exoelectro-
E-mail address: cpyu@ntu.edu.tw (C.-P. Yu).

https://doi.org/10.1016/j.psep.2019.03.016
0957-5820/© 2019 Institution of Chemical Engineers. Published by Elsevier B.V. All rights reserved.
84 B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91

gens on the anode, which will in turn produce electrons to reach content and 2.2 g L−1 total nitrogen (indicating the summation of
the cathode through an external circuit. For a typical two-chamber Kjeldahl nitrogen, nitrite and nitrate).
MFC, the anodic and cathodic chamber are separated by a proton
exchange membrane that allows the transport of protons between
the anode and cathode (Wang et al., 2017). On the cathode, pro-
tons and electrons simultaneously react while reducing oxygen 2.2. Microbial fuel cell reactor construction and operation
to water when oxygen is used as the terminal electron acceptor
(Feng et al., 2013; Rabaey et al., 2004; Rahimnejad et al., 2011). The two-chamber MFCs were constructed using two 120 mL
As shown in the previous studies, several operational factors have glass bottles. The carbon felts (4 cm × 2 cm × 0.5 cm thick; sur-
effects on MFC performances, such as MFC configuration, scales, face area 22 cm2 ) were used as electrodes. Before use, the carbon
materials of the electrode, electron donors, anolyte pH, and so on felt electrodes were submerged in 1 M HCl for 24 h and then
(Feng et al., 2014; Madani et al., 2015; Nastro et al., 2017). The thoroughly rinsed using miliQ water. The MFC chambers were
cathodic electron acceptor is also critical for the current produc- separated by a cation exchange membrane of polyethylene styrene-
tion in MFCs. Ferricyanide possesses a high solubility of 464 g L−1 divinylbenzene (Grion 0011 V, Hangzhou Grion Environmental
at 20 ◦ C (Knwong (2004) in the water, which is significantly higher Technology Co., China) pretreated by soaking in 10% sulfuric acid
than that of oxygen (7.6 mg L−1 ) at 20 ◦ C (Emsley (2001)), and this for 24 h then washed with milliQ water. MFCs were operated
characteristic provides a faster kinetic for ferricyanide reduction into two groups: Nutrient medium with FW (FWM) and nutrient
on the cathode, although oxygen possesses higher redox potential medium with FW plus Wolfe’s vitamin solution and mineral solu-
than ferricyanide does (i.e., 0.84 and 0.36 V vs. standard hydrogen tion (FWVM). The anode compartments were filled with 120 ml of
electrode, respectively) (Li et al., 2017a). In addition to oxygen and nutrient medium containing the following composition (per liter
ferricyanide, potassium permanganate with higher redox poten- of miliQ water): 10 g FW (wet weight), 11.55 g Na2 HPO4 ·12H2 O,
tial (i.e., 1.52 V vs. standard hydrogen electrode) also contributed to 2.77 g NaH2 PO.2H2 O, 0.31 g NH4 Cl, 0.13 g KCl. For the FWM group
good performances when it was used on the cathode in the previous it used the medium mentioned above and for the FWVM group the
studies. When MFCs were treating synthetic wastewater (Cai et al., nutrient medium was supplement with 12.5 mL of Wolfe’s vita-
2016) or LB broth (Pandit et al., 2011) in the anodic chamber, the min solution (2.0 mg biotin, 2.0 mg folic acid, 10.0 mg pyridoxine
ones using permanganate as the cathodic electron acceptor could hydrochloride, 5.0 mg thiamine-HCl, 5.0 mg riboflavin, 5.0 mg nico-
produce higher power densities than the ones using ferricyanide tinic acid, 5.0 mg calcium D-(+)-pantothenate, 0.1 mg vitamin B12,
(Cai et al., 2016; He et al., 2015). 5.0 mg p-Aminobenzoic acid and, 5.0 mg thioctic acid, in per liter of
MFCs have been proven to use diverse substrates to produce milliQ water) and 12.5 ml of Wolfe’s mineral solution (1.5 g nitrilo-
electricity, such as different wastewater, sewage sludge, biomass, triacetic acid, 3.0 g MgSO4 ·7H2 O, 0.5 g MnSO4 ·H2 O, 1.0 g NaCl, 0.1 g
manure, and etc. Recently, studies have shown that it is feasible to FeSO4 ·7H2 O, 0.1 g CoCl2 ·6H2 O, 0.1 g CaCl2 , 0.1 g ZnSO4 ·7H2 O, 0.01 g
use FW as the substrate to produce electricity in MFCs (Li et al., CuSO4 ·5H2 O, 0.01 g AlK(SO4 ) 2 ·12H2 O, 0.01 g H3 BO3 and 0.01 g
2016; Miran et al., 2016; Colombo et al., 2017). In the MFC fed Na2 MoO4 ·2H2 O, adjust to pH of 6.5 in per liter miliQ water) pre-
with FW, the organic characteristics of FW will significantly affect pared according to recipe used by Jia et al. (2013). Finally, the pH
the electricity generation. Among all the FW degradation stages, values of the diluted FWs were 7 without any adjustment.
organic matters hydrolysis is recognized as the rate determining The MFCs were first operated using ferricyanide (50 mM) and
step. Therefore, understanding the FW characteristics (including then potassium permanganate (50 mM) in phosphate buffer solu-
COD, TOC, polysaccharide and protein concentrations) and their tion (6.7 g Na2 HPO4 ·12H2 O, 1.5 g KH2 PO4 per liter of milliQ water)
biodegradability are critical for MFC operation (Ma et al., 2014; (Sharma et al., 2016) as the catholyte. The anolyte was inoculated
Jia et al., 2013). However, due to our limited knowledge regarding with sludge (mixed liquid suspended solid 3.45 g L−1 ) collected
FW treatment that may form a bottleneck in the future develop- from Jimei wastewater treatment plant (Xiamen, China). The tita-
ment, in this study we evaluated the effects of additional nutrients nium wires (0.5 mm in diameter) were attached on the carbon felts
and different cathodic electron acceptors (ferricyanide and per- as current collectors. The external resistance was set to be 1 k
manganate) on electricity generation from FW in MFCs. To better during operation. Reactors were running in repeated batch mode
enhance the MFC outputs for future application, the FW-fed MFC at an ambient temperature. When the voltage decreased to less
was connected to a power management system (PMS) to increase than 40–55 mV, the liquid was entirely taken out of each batch
the voltage output to a sufficient level, using supercapacitors to and a portion was saved for analyzing COD, TOC, TN, polysaccha-
accumulate MFC energy over a certain period and provide inter- rides, and total protein; subsequently each anodic chamber was
mittent electricity to loads (Yang et al., 2012). Furthermore, to refilled with the correspondent fresh media (120 mL) to implement
explore the microbial communities involved in electricity gen- another cycle.
eration from FW, we used the 16S rRNA gene high-throughput The fresh medium of anode was purged with N2 for 40 min (flow
sequencing approach to analyze the microbial communities on the rate 1.5–2 ml/min) to maintain its anaerobic condition. MFCs under
anodes. The results in this study will be beneficial for enhancing each operation condition were operated in duplicate.
the conversion of bioelectricity from FW in MFCs.

2. Materials and methods 2.3. Configuration of the power management system

2.1. Food waste collection In the experiments, the electric circuit of intermittent charging
mode was employed and the integrated circuit chip was designed
FW collected from the canteen of the Institute of Urban Envi- according to the previous study (Meehan and Gao (2011); Mo et al.,
ronment, Chinese Academy of Sciences in Xiamen, was used as the 2013). The PMS was consisted of the following parts: a charge pump
substrate in MFCs. At the outset, bones were removed from FW, (Seiko S-882Z22), a supercapacitor (SAMXON), a DC-DC boost con-
and then an electrical blender was used to pulverize the FW. The verter (Yunhui MAX1674) and two solid-state switches (Yunhui
pretreated FW had 250 g L−1 chemical oxygen demand (COD), 68 g P-Channel MOSFET AO3401 and N-Channel MOSFET AO3402). The
L−1 polysaccharide, 63 g L−1 total organic carbon (TOC), 81% water schematic diagram is shown in Fig. S1.
B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91 85

2.4. Analytical methods

Samples from the anodic chambers were analyzed to know total


COD, polysaccharide, protein, TOC and TN. COD was analyzed by
using the COD measurement system and kit (Lianhua Technology,
Beijing, China). TOC and TN were analyzed by (TOC-Vcph analyzer,
Shimadzu, Japan). Proteins were quantified using bicinchoninic
acid assay and the absorbance was measured at 562 nm (Seo
et al., 2008). The polysaccharide was measured using the anthrone
method (DuBois et al., 1956). Colorimetric analysis was done by the
microplate reader SpectraMax M5 (Molecular devises, USA). Closed
circuit cell voltage (CCV) was continually recorded every 10 min
using a data acquisition system (UBS7660-B ZTIC, China) during-
operation. The half-cell potentials were determined by measuring
the potential differences between a reference electrode (Ag/AgCl)
and the anode or cathode, respectively, using a digital multi-meter
MSS830L® (Mastech, Shanghai, China). The polarization curve was
examined by varying the external-circuit resistance in a range of
101 -104 , which is able to reveal the maximum power density of
the MFCs. The power density (P) was calculated following the equa-
tion: P = E×I /A where E, I, and A indicate the CCV, current, and anode
surface area, respectively. The current density (j) were calculated
by dividing the obtained current with the anode surface area (Goud
et al., 2011). Columbic efficiency (CE) was calculated as follow as:

8 idt
CE = × 100
FVanode COD

where, F is the Faraday constant, Vanode is the working volume of


anode chamber, COD (<0) is the change in the mass concentration
of COD and 8 is the equivalence factor that converts the mass con-
centration of COD into the moles of oxygen-equivalent electrons
(Logan et al., 2006; Madani et al., 2015).
A Zeiss LSM 710 confocal laser scanning microscopy (CLSM,
ZEISS, CA, USA) was used to get image of the anode biofilm. CLSM
images of the biofilm on a carbon-felt anode were taken from
the MFC after stable power generation. Cells were stained using
a LIVE/DEAD® BacLight Bacterial Viability Kits to show live (green
fluorescent) and dead (red fluorescent) cells.

Fig. 1. Voltage-output profiles of MFCs with external resistance R = 1000  in three


2.5. DNA extraction, PCR amplification and high throughput FW-feeding cycles. (A) MFCs using ferricyanide as the cathodic electron acceptor;
sequencing (B) MFCs using permanganate as the cathodic electron acceptor; solid line, feeding
FWVM; dashed line, feeding FWM.
Samples were collected from the carbon-felt anodes of MFCs
after around 8 months of operation. The V4-V5 region of the reduction in MFCs (Rabaey et al., 2003). With an initial COD of
prokaryotic 16S rRNA gene were amplified using the universal 2.5 g L−1 , the electricity was immediately generated either from
primer 515 F (5 -GTG YCA GCM GCC GCG GTA-3 ) and 907R (5 - the FWM or FWVM MFCs, but it took 3 months to have stable max-
CCG YCA ATT YMT TTR AGT TT-3 ) (Hu et al., 2017), with a PCR imum voltage output. Fig. 1a shows the CCV changes of FWM and
condition of 95 ◦ C for 3 min followed by 25 cycles of 95 ◦ C for 45 s, FWVM MFCs with time. In each cycle, after refreshing the FW media
50 ◦ C for 60 s, 72 ◦ C for 90 s, and 72 ◦ C for 10 min. The triplicate PCR in the anodic chamber and catholyte in the cathodic chamber, the
products were gel-purified and pooled. Equimolar PCR products CCV immediately jumped to a maximum value around 600 mV
were pooled and sequenced in the Majorbio Bio-Pharm Technol- (e.g. 603 ± 25 mV within the three cycles for FWM; 600 ± 20 mV for
ogy Co., Ltd. (Shanghai, China) on a MiSeq platform (Illumina Inc., FWVM), and then gradually decreased due to nutrient depletion in
San Diego, CA, USA) with paired-end approach (2 × 300 bp). The the anode compartment (Logan et al., 2006).
sequences produced in this experiment were deposited in the NCBI MFCs were further shifted to use 50 mM potassium perman-
short reads archive database under BioProject number 433072. ganate as the catholyte, with the same COD concentration in the
anode chamber as used in the ferricyanide MFCs, and the electric-
3. Results and discussion ity was able to be generated either from the FWM or FWVM. Fig. 1b
shows the CCV changes of FWM and FWVM MFCs with time. In each
3.1. Power generation of MFCs with ferricyanide and cycle, after refreshing the FW media in the anodic chamber and
permanganate as the catholyte catholyte in the cathodic chamber, the CCV immediately increased
to a maximum value of more than 700 mV (e.g. 775 ± 21 mV within
Experiments were carried out to compare the performance of the three cycles for FWM; 720 ± 17 mV for FWVM), and then grad-
FWM and FWVM MFCs using 50 mM potassium ferricyanide in the ually decreased.
cathodic chamber. Several studies have shown the good perfor- The maximum CCV obtained using permanganate as the
mance of ferricyanide by enhancing the efficiency of the cathodic catholyte was higher than that obtained using ferricyanide, because
86 B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91

the redox potential of potassium permanganate (i.e., 1.523 V) (Kong


et al., 2010) is higher than that of ferricyanide (i.e., 0.77 V) (Kong
et al., 2010). Generally, the results obtained from our study are
higher than those obtained from the previous MFC studies treating
FW using oxygen as the cathodic electron acceptor. For example,
a 296 mV CCV was generated by an air-cathode MFC fed with ini-
tial FW COD of 4.9 g L−1 (Jia et al., 2013), and a 50 mV CCV was
generated by an air-cathode MFC fed with different food-industry
residues (including mixed kitchen waste, whey, fish, pulp, and the
initial COD = 3.7 g L−1 as substrate) (Colombo et al., 2017).

3.2. Coulombic efficiency and power density

The CE is an important indicator used to estimate how efficiently


the electricity was produced from the consumed COD (Logan et al.,
2006). The CE of each run was calculated according to the measured
current density and COD profiles. The average CE of our ferricyanide
MFCs was estimated to be 13 ± 2%, and 28 ± 20% for FWM and
FWVM, respectively; the average CE of permanganate MFCs was
estimated to be 14 ± 8%, and 12 ± 3% for FWM and FWVM, respec-
tively. It showed that catholyte ferricyanide and permanganate did
not cause significant influence on CE (t-test, P > 0.05). We hypoth-
esize that oxygen diffusion to the anodic chamber, unexpected
electron consumption by methanogens, metabolic generation and
incapability of bacteria in converting all substance to electricity
could potentially cause the decrease of CE (Kim et al., 2011; Logan,
2012; Mansoorian et al., 2016; Rikame et al., 2012).
According to polarization curves, the maximum power densities
for the ferricyanide MFCs fed with FWM and FWVM were 317 and
337 mW m−2 at the CCV of 374 and 385 mV (Fig. 2a); the maximum
power densities for the permanganate MFCs fed with FWM and
Fig. 2. The polarization (solid square) and power density (solid circle) curves (using
FWVM were 422 mWm−2 and 410 mW m−2 , at the CCV of 431 and external R = 1000 to 10 ) under different operational conditions. (A) MFCs using
540 mV, respectively (Fig. 2b). The maximum power densities in ferricyanide as the cathodic electron acceptor; (B) MFCs using permanganate as the
our MFCs were higher than those in the open-air cathode MFCs cathodic electron acceptor; red symbols, feeding FWVM; black symbols, feeding
feeding with composite FW (110 mW m−2 , initial COD of 330 g L−1 ) FWM (For interpretation of the references to colour in this figure legend, the reader
is referred to the web version of this article.).
(Goud et al., 2011) and 170 mW m−2 (Mohan and Chandrasekhar,
2011), and in MFCs using manganese dioxide as cathodic electron
acceptor feeding with the mixture of fruit, vegetable wastes, and Higher organics removal may be attributed to a better microbial
soil (5 mW m−2 ) (Md Khudzari et al., 2016). On the other hand, growth on the anode surface (Goud et al., 2011; Rikame et al., 2012).
the maximum power density obtained in an open-air cathode MFC The maximum COD removal in our MFCs was 85 ± 6%, which per-
feeding with FWVM (initial COD of 3.2 ± 0.4 g L−1 ) was 556 mW formed better than the reported investigation which claimed a 70%
m−2 (Jia et al., 2013), which was close to our study. These results removal in MFCs fed with FWs at different organic loading rates (Jia
demonstrated that not all the organic ingredients in the FW might et al., 2013), but less than the study operating a dual-chamber MFC
be easily and readily degradable in MFCs, which would limit the fed with FW leachate (90% COD removal at the optimum condition)
power generation in different cases (Lee et al., 2008). (Rikame et al., 2012). In the present investigation, we found that the
carbohydrate was better removed than protein, which suggested
3.3. Organic matter removal in MFCs that the carbohydrate was preferentially used by microorganisms
as compared to protein. It is possibly due to that, the proteins hold
Different compositions removals of FW in MFCs are shown in complicated molecular structures that limit the microorganisms to
Fig. 3 and Table S1. The average COD removals were 85 ± 6 and achieve a decent degradation (Rajesh and Ghangrekar, 2016).
55 ± 23% obtained from FWM and FWVM MFCs using ferricyanide
as the cathodic electron acceptor. The total protein removals were 3.4. Energy harvesting using the power management system
73 ± 7 and 88 ± 19% for FWM and FWVM MFCs, respectively. The
results also revealed that the TOC and TN removals in FWM MFCs In order to evaluate the long-term electricity generation of
were significantly higher than those in FWVM MFCs (t-test, P < MFC fed with FW, an intermittent energy harvesting approach
0.05). Additionally, we found that total polysaccharide removal was was used for MFCs devices to charge capacitors. Energy was har-
similar between FWM and FWVM MFCs under closed circuit condi- vested from the FWM MFCs with ferricyanide as the catholyte (we
tions. Fig. 3b shows the average organics removals of permanganate observed long-term operation of 50 mM potassium permanganate
MFCs. The average COD removals were 69 ± 18% and 78 ± 10% for could cause damage to the cation exchange membrane) and the
FWM and FWVM MFCs, respectively. Polysaccharide removals were 5.5 V supercapacitor of 0.47 F or 1 F was used as the energy stor-
88 ± 5 and 84 ± 17% for FWM and FWVM MFCs. In addition, the pro- ing device. Fig. 4 shows the charging and discharging behavior of
tein removals were 76 ± 9 and 46 ± 28% for FWM and FWVM MFCs. the PMS by demonstrating the voltage changes of the MFC, the
TOC and TN removals were similar between FWM and FWVM MFCs. supercapacitor and the boost converter within one MFC-feeding
The organic (COD, TOC, polysaccharide and protein) removals in fer- cycle.
ricyanide and permanganate MFCs were not significantly different The charge pump drew current from the MFC with the MFC
(t-test, P > 0.05). input voltage ranging from 0.4 to 0.6 V (blue line in Fig. 4) and
B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91 87

stored the energy in the supercapacitor (green line in Fig. 4). Dur-
ing the charging stage, when the voltage of the supercapacitor was
lower than 2.2 V, the charge pump opened the switches between
the supercapacitor and the boost converter, which makes them dis-
connected from each other. Then the capacitor will be charged by
the MFC through the charge pump. Until the supercapacitor voltage
reaches 2.2 V, the charge pump would be shut down but then the
connection between the supercapacitor and boost converter would
recover to enable the electric energy flow from the supercapacitor
to boost converter. Finally, the voltage of the PMS will be boosted
to 3.4 V (red line in Fig. 4) which renders the bioelectricity a suf-
ficient level to drive some small electronic devices. Because of the
energy consumption by load (i.e., electronic devices), the superca-
pacitor voltage will drop from 2.2 to 1.6 V, and hence the switches
between the supercapacitor and boost converter will be shut off to
change the discharging into charging stage. The boost converter will
not start up again until the supercapacitor is charged to 2.2 V. This
charging and discharging process will be repeated until the charg-
ing voltage of MFC dropped to below 300 mV, due to the substrate
depletion. Charging the 0.47 F capacitor took around 3.2 h (Fig. 4a)
in each cycle, while charging the 1 F capacitor took approximately
9 h (Fig. 4 b). Our results demonstrated that the produced bioelec-
tricity from food waste fed MFCs can be successfully harvested for
driving suitable electronic devices.

3.5. Analyses of microbial communities on the anode


Fig. 3. Average removal efficiencies of COD, protein, polysaccharide, TOC, and TN
of FW in the MFCs. (A) MFCs using ferricyanide as the cathodic electron acceptor; After around 8 months of operation of MFCs, the biofilms were
(B) MFCs using permanganate as the cathodic electron acceptor; red bars, feeding scratched away from the electrodes to analyze the microbial com-
FWVM; red pattern bars, feeding FWM (For interpretation of the references to colour munity composition. The operational taxonomic units (OTUs) were
in this figure legend, the reader is referred to the web version of this article.).
determined according to the results analyzed by high through-

Fig. 4. Voltage changes of MFC (blue line), supercapacitor (green line), and boost converter (red line) during the charge-discharge process in the PMS. (A) with 0.47 F
supercapacitor, (B) with 1 F supercapacitor (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.).
88 B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91

Fig. 5. Relative abundance of dominant bacterial phyla/classes in each anode sample. MFCs fed with FWM in duplicate (FWM1 and FWM2) and FWVM in duplicate (FWVM1
and FWVM2) under closed circuit condition.

put sequencing. The microbial communities in different samples


are mainly categorized into 9 phyla. The dominant phyla in MFCs
were Firmicutes (38.7%), Bacteroidetes (28.5%) and Proteobacte-
ria (28.1%) (Fig. 5). Although different anodic microbial community
structures for different FW substrates were observed, but the repli-
cate MFCs fed with the same FW substrate also showed different
anodic microbial community, likely due to the stochastic effect with
the complexity of FW mixtures. At the class level, Bacilli (28%) and
Bacteroidia (14%) dominated the microbial community, followed
by the class Deltaproteobacteria (10%) and Gammaproteobacteria
(6%) (Fig. 6a). The remaining classes accounted for similar percent-
age (2–5%) as shown in Fig. 6a. At the genus level shown in Fig. 6b,
Geobacter contributed to the most within the whole microbial com-
munity (5%), followed by Petrimonas (4%), Erysipelotricha (4%) and
Escherichia-Shigella (4%), respectively.
FW, which contains various organic substances such as carbo-
hydrates, proteins and some inorganic salts, is capable of enriching
high diversity of microorganisms in the MFCs. Among the domi-
nant bacterial genera identified in our MFCs, the Geobacter species
have been the most studied exoelectrogenic bacteria to date.
This microorganism also possesses the potential on bioremedia-
tion with concomitant electricity production (Poddar and Khurana,
2011), which was widely found in the mixed culture commu-
nity of MFCs (Commault et al., 2015). Besides, several genera of
the Erysipelotrichaceae were also reported to be electroactive in
biofilms (Rago et al., 2017). In addition to exoelectrogenic microor-
ganisms, the genus Petrimonas (contributed to 3% of the total
community in this study) was reported to be able to oxidize or
ferment substrates like brewery waste (Chen et al., 2017; Miran
Fig. 6. Percentage of different classes (a) and genera (b) to the whole bacterial
et al., 2015). It is reasonable that some populations of bacteria in community.
MFCs may not be directly involved in current production but in
decomposing complicated organic substrates into simple metabo-
lites which can be further utilized by exoelectrogens (Patil et al.,
mentative bacteria have developed an effective consortium on the
2009). Consequently, it is not surprised that Bacteroides and Fir-
electrode, the goal of directly generating electric power from FW
micutes, which could do critical work to provide small molecule
could be achieved.
metabolites, were found to be dominated in MFC studies (Jia et al.,
Fig. 7 shows the confocal laser scanning microscopy images of
2013; Wrighton et al., 2008; Rismani-Yazdi et al., 2013), and were
live and dead cells in anode biofilm. Fig. 7(d) (the merged image of
also frequently found in anaerobic digestors and even human
Fig. 7(a), (b), (c)) shows that anode biofilm contained a mixture of
intestines (Zamanzadeh et al., 2016; Thomas et al., 2011). Com-
both living microbial cells (green fluorescence) and dead microbial
bining the microbial community obtained with those reported in
cells (red fluorescence). Fig. 7 (a) shows the dead microbial cells
previous studies, it is shown that once the exoelectrogenic and fer-
which seemed irregularly scattered and some cells of them were
B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91 89

Fig. 7. Confocal laser scanning microscopy images. Dead cells (red fluorescence) (a), live cells (green fluorescence) (b), bright-field image (c), merged image of a, b, c (d) (For
interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.).

not attached on the electrode surface but present as spherical cocci which holds potential to compete with other alternative FW treat-
and rod-shaped bacilli. Fig. 7 (b) reveals a dense population of living ment technologies and further development is warranted.
microbial cells and a cluster of cells or biofilm could be observed
although some living cells also randomly scattered. Author contributions

B.A. and C.-P.Y. conceived and designed the experiments; B.A.


4. Conclusions
and J.L. performed the experiments; B.A., S.-L.L., H.A.M., A.H. and
C.-P.Y. analyzed the data; B.A., S.-L.L., V.S.-T., J.L. and C.-P.Y. wrote
The present study demonstrated simultaneous organic matter
the paper.
degradation and electricity generation using MFCs fed with FW
as the substrates. It was observed that MFCs fed with FWM and
permanganate as the catholyte could achieve the highest closed Conflicts of interest
circuit voltage and maximum power density at 775 ± 21 mV and
422 mW m−2 , respectively. The microbial communities on the The authors declare no conflicts of interest in relation to this
MFC anodes showed great varieties and contained the mixture of work.
exoelectrogenic and fermentative bacteria. The PMS test demon-
strated that electricity generated from FW-fed MFCs could be Acknowledgments
successfully harvested to provide intermittent electricity to drive
suitable electronic devices. These results therefore render the MFC The authors would like to express their gratitude for the finan-
a multi-functional device which works both for FW treatment and cial support provided by the STS Project of Fujian-CAS (2016T3004),
electricity production. In summary, this study demonstrates the the National Natural Science Foundation of China (41673099,
capability of generating bioelectricity from the FW in the MFCs 31500420), the Sino-Latin America Young Scientist Exchange Pro-
90 B. Asefi et al. / Process Safety and Environmental Protection 125 (2019) 83–91

gram of the Ministry of Science and Technology of China, and the Madani, S., Gheshlaghi, R., Mahdavi, M.A., Sobhani, M., Elkamel, A., 2015. Optimiza-
VIE-UIS project 5487. tion of the performance of a double-chamber microbial fuel cell through factorial
design of experiments and response surface methodology. Fuel 150, 434–440.
Mansoorian, H.J., Mahvi, A.H., Jafari, A.J., Khanjani, N., 2016. Evaluation of dairy
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