Bioresource Technology 256 (2018) 11–16

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Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

Using a tubular photosynthetic microbial fuel cell to treat anaerobically T

digested effluent from kitchen waste: Mechanisms of organics and
ammonium removal
⁎
Haiyan Peia,b, , Zhigang Yanga, Changliang Niea, Qingjie Houa, Lijie Zhanga, Yuting Wanga,
Shasha Zhanga
a
School of Environmental Science and Engineering, Shandong University, No. 27 Shanda Nan Road, Jinan 250100, China
b
Shandong Provincial Engineering Centre on Environmental Science and Technology, No. 17923 Jingshi Road, Jinan 250061, China

A R T I C L E I N F O A B S T R A C T

Keywords: Anaerobically digested effluent from kitchen waste (ADE-KW) was used herein as the substrate of a tubular
Tubular photosynthetic microbial fuel cell photosynthetic microbial fuel cell (PMFC) for power production, and also, after being diluted, as a medium for
Anaerobically digested effluent cultivation of algae in the cathodic chamber. Adding 3 mg/L phosphorus to the catholyte could efficiently en-
Algal biomass hance the algal growth and the PMFC performance. About 0.94 g/L algal biomass and 0.57 kWh/m3-ADE-KW
Organics composition
bioelectricity were obtained from the PMFC. Soluble microbial byproduct-like material and aromatic proteins
Ammonium migration
were the dominant organics in the ADE-KW, which were readily degradable in the system. About 79% of the
1550 mg/L ammonium in the anolyte transferred to the catholyte through the cation exchange membrane. The
ammonium was removed mainly as electron acceptors at the cathode after being oxidized by oxygen, whereas
algal assimilation only account for about 14.6% of the overall nitrogen.

1. Introduction
Kitchen waste constitutes a large component (30–50%) of municipal
solid wastes (Shin et al., 2015; Levis and Barlaz, 2011). Anaerobic di-
gestion has been proved to be an effective technology to manage
kitchen waste and also produce abundant energy resources like me-
thane (Huang et al., 2015). Nonetheless, anaerobically digested effluent
from kitchen waste (ADE-KW) is still of severe environmental concern
for its high content of nutrients (Shin et al., 2015). Microbial fuel cells
(MFCs) are bioelectrochemical systems that have been recommended to
complement anaerobic digestion for ADE-KW treatment (Li et al.,
2013a; Li et al., 2013b). However, some disadvantages limit the prac-
tical application of MFC, such as incapable of ammonium removal and
energy-intensive (e.g. aeration).
A tubular photosynthetic microbial fuel cell (PMFC) system, using
an algae-assisted cathode, is a promising technology that can not only
convert chemical energy stored in organic matter to electric energy but
also recover nutrients using microalgal technology. The oxygen pro-
duced by the photosynthesis of algae will save the additional energy
that would otherwise be needed for aeration. Previous studies demon-
strated that it is feasible to cultivate algae in wastewater, such as di-
luted ADE-KW, to produce biodiesel (Shin et al., 2015; Vasconcelos
Fernandes et al., 2015; Pei et al., 2017). Thus, using diluted ADE-KW as
algal culture medium, which also functions as the catholyte, can si-
multaneously achieve organics removal, nutrient removal and bioe-
nergy production. Additionally, the tubular PMFC that a MFC was in-
stalled in a photosynthetic bioreactor (PBR) allows the algae to grow in
the “U” shape sector so that the light is more accessible (Xiao et al.,
2012; Ma et al., 2017). Furthermore, the large effective area of cation
exchange membrane (CEM) can reduce the internal resistance of the
PMFC markedly, which was beneficial for power generation (You et al.,
2006).
ADE-KW was characterized with high nutrients (ammonium) and
salinity (Pei et al., 2017). Thus, recovery of nitrogen from ammonium-
rich ADE-KW was a goal of this study. It is notable that the ammonium
could transfer from the anodic chamber to the cathodic chamber
through the CEM, especially in the tubular PMFC, in which the CEM has
a large specific surface area of about 23 m2 CEM m−3 anolyte. The ef-
fect of current generation is a driving force for ammonium transpor-
tation from an anodic chamber to a cathodic chamber. Diffusion is
another reason for ammonium transportation, especially in ammonium-
rich anolyte (Haddadi et al., 2013). Thus, it is expected that vast
amounts of ammonium would transfer into the catholyte which could
function as the nutrient for algal growth. The ammonium in the

⁎
Corresponding author at: School of Environmental Science and Engineering, Shandong University, 27 Shanda Nan Road, Jinan 250100, China.
E-mail address: haiyan@sdu.edu.cn (H. Pei).

https://doi.org/10.1016/j.biortech.2018.01.144
Received 18 November 2017; Received in revised form 28 January 2018; Accepted 31 January 2018
Available online 02 February 2018
0960-8524/ © 2018 Elsevier Ltd. All rights reserved.
H. Pei et al.
catholyte can also be oxidized and then removed as electron acceptors
on the cathode. To the best of our knowledge, the study was the first
attempt to study the ammonium migration effect in an algae-assisted
bioelectrochemical system.
It is estimated that the N/P (molar) ratio of ADE-KW was more than
100 which much higher than the ideal N/P ratio for algal growth
(Chisti, 2007). Phosphorus (P) is the second most frequent macro-
nutrient that limits algal growth after nitrogen (Solovchenko et al.,
2016) Therefore, it is necessary to introduce additional phosphorus to
the diluted ADE-KW to regulate the N/P ratio of the culture. In this
study, anaerobically digested effluent from kitchen waste (ADE-KW)
was used as the substrate for bioelectricity generation in the anodic
chamber of a tubular PMFC. Diluted ADE-KW was used as the micro-
algal culture, and also functioned as the catholyte. The objectives of this
study were to: (1) optimize the performance of PMFC by varying
phosphorus concentration; (2) reveal the mechanisms of organics re-
moval in the PMFC with a substrate of ADE-KW; (3) study the ammo-
nium removal processes in an algae-assisted bioelectrochemical system.
2. Materials and methods
2.1. Experimental set-up
The tubular Plexiglas anode chamber of the PMFC had a working
volume of 350 mL (height 200 mm, diameter 60 mm) and ten rectan-
gular holes (height 160 mm, width 5 mm) on the anode chamber for
cation exchange between anolyte and catholyte. The cathode chamber
(working volume 1500 mL) consisted of a cylindrical section (height
200 mm, diameter 13 mm) joined to a conical section, and also func-
tioned as an algal bioreactor (Fig. 1). A cation exchange membrane
(CEM) was wrapped around the tubular anodic chamber to separate the
anodic and cathodic chambers, and then a layer of carbon cloth was
wrapped around the CEM to function as the cathode. The anode was a
piece of carbon cloth (height 160 mm, width 40 mm) interwoven with
titanium wires. Prior to use, the carbon cloth and CEM were pretreated
to remove possible trace metal and microbial contamination (Ma et al.,
2014). The CEM was pretreated by immersion in the 3% H2SO4 for 4 h
at room temperature and then washed with deionized water. The
carbon cloth was pretreated by immersion in the 1 M HCl and 1 M
NaOH for 24 h, respectively. After that, they were washed with
Fig. 1. Schematic of tubular photosynthetic microbial fuel cell (PMFC) for ADE-KW
treatment.
12
Bioresource Technology 256 (2018) 11–16
deionized water as previously described (Hou et al., 2016). The anode
and cathode were connected by titanium wires with an external re-
sistance of 200 Ω.
The anode chambers were fed with ADE-KW (Shandong Shifang
Environmental Protection and Bio-Energy Co.) that had been filtered
through eight layers of gauze to remove insoluble solids before being
used. The pore size of the gauze is 0.6 mm (diameter). The concentra-
tions of pollutants in the ADE-KW were as follows: 4530 ± 108 mg/L
COD, 1550 ± 20 mg/L NH4+-N, 15.0 ± 4.8 mg/L NO3−-N,
2.5 ± 0.6 mg/L NO2−-N and 26.7 ± 3.2 mg/L TP. The green algae
Golenkinia sp. SDEC-16 (Accession No.: KT180320) was cultivated in
the cathodic chambers with diluted ADE-KW. Before the experiment,
the ADE-KW was firstly centrifuged (5000g, 10 min) to reduce the dark
colour of ADE-KW, and a concentration of 4% (v/v) ADE-KW diluted
with deionized water was specified as the medium for algae.
In order to enhance the algal growth, extra P was added into the
catholyte. The P levels were boosted by 1, 3, 6 and 9 mg/L through
addition of K2HPO4 to the catholyte of the relevant systems. The diluted
ADE-KW (with a P concentration of about 0.7 mg/L) without extra P
addition was set as the control system. Before the experiment, 0.1 M KCl
and 0.1 M HCl were used to maintain similar pH and conductivity levels
of the catholytes in different systems. The initial values of the pH of
anolyte and catholyte were about 8.1 and 7.8, respectively. The initial
values of conductivity of the anolyte and catholyte were about 0.56 mS/
cm and 1.25 mS/cm, respectively. An initial algal biomass concentra-
tion of 0.15 ± 0.1 g/L was inoculated into the cathodic chambers. The
anodic chamber was inoculated with 20 mL anaerobic sludge collected
from a municipal wastewater treatment plant in Jinan, China. A con-
tinuous illumination of 100 μmol m−2 s−1 was provided by a row of
fluorescents lamps during the experiment. Room temperature was
control at 25 ± 1 °C. Continuous mixing (300 rpm) was provided in the
cathodic chamber using a magnetic stirrer.
2.2. Analytical methods
2.2.1. Bioenergy analysis
The voltage across the external resistance was recorded with a data
acquisition system (Keithley Instruments 2700, USA). The volumetric
power density (W/m3) normalized to the anolyte volume was calcu-
lated by dividing the power (W) by working volume of the anodic
chamber (m3). The Coulombic efficiency (CE) was calculated from the
equation:
t
8 ∫0 Idt
CE =
FVA ΔCOD
where VA is the effective anode volume, I is the current, ΔCOD is the
change of COD over time t, and F is the Faraday constant (96,485 C/
mol). The lipid contents of the algae were measured using a chloro-
form/methanol mixture (2:1, v/v) (Pei et al., 2017). Energy embedded
in lipids was estimated based on a conversion efficiency of 30% from
lipid (energy of lipid is about 37,800 J/g) to electricity excluding the
energy produced from biomass (Xiao et al., 2012). The total energy
(kWh) produced in the form of electricity and lipid was normalized to
the volume of consumed ADE-KW (m3).
2.2.2. Ion transfer
When current is generated, ion transfer to satisfy charge neutrality
would cause cations to migrate from the anodic chamber to the
cathodic chamber through the CEM. Hence, the total ion transfer driven
by current generation can be expressed by the following equation
(Haddadi et al., 2013):
n
dQ
F
= ∑ Zi Mi
i
in which, Q is cumulative coulombs (C), F is the Faraday constant
H. Pei et al.
(96,485 C/mol), i is ion exchanged between compartments, Z is the ion
valence, and M is the ion amount (mol).
2.2.3. Dissolved organic matter
Different organic components are consistent with different max-
imum excitation and emission wavelength. Fluorescence ex-
citation–emission matrices (EEMs) can be used to characterize dis-
solved organic matter in the ADE-KW. In this study, the EEMs were
determined using a luminescence spectrometer (5J2-004, Hitachi,
Japan) by scanning the samples over excitation wavelengths from 220
to 450 nm and emission wavelength from 250 to 550 nm. The ADE-KW
samples were diluted by a factor of 10 times to avoid the inner filtering
effect.
2.2.4. Algal biomass
The growth of algae was evaluated in terms of dry biomass in 20 mL
samples of algae suspension. Firstly, the algal suspension was cen-
trifuged at 5000 rpm for 10 min, then the supernatant was returned to
the reactors and remaining pellets were dried to constant weight. The
algae were separated by centrifuge (TDL-8M, Luxiangyi, China) and
dried using a lyophilizer (Eyela FDU-1200, Tokyo Rikakikai Co.,
Japan). About 0.1 g of dry powdered algae was digested with H2SO4
and H2O2, and the samples were filtered through a 0.45 µm membrane
to analyze mass fractions of N and P in the algae.
2.2.5. Chemical and physical analysis
The concentrations of metal ions were determined using an in-
ductively-coupled plasma optical emission spectrometer (180-80,
Hitachi, Japan). Light intensity was measured using a photometer (TES-
1332A, TES, Taiwan). Total nitrogen (TN), ammonium, nitrate, nitrite
and total phosphate (TP) were determined using a spectrophotometer
(UV2450, Shimadzu, Japan) after filtration through 0.45 μm filters.
Chemical oxygen demand (COD) was measured according to the stan-
dard dichromate oxidation method. Dissolved oxygen (DO) was mea-
sured with a DO meter (HQ30d, Hach, U.S.A.). The pH was measured
with a pH meter (pHS-3C, INESA, China).
3. Results and discussion
3.1. Production of algae and power generation
3.1.1. Algal biomass
The results shown in Fig. 2a indicated that the algal growth was
limited under the control conditions, i.e. without extra P addition. After
Fig. 2. Algal growth curves and power density of the tubular photosynthetic microbial fuel cell (PMFC).
13
Bioresource Technology 256 (2018) 11–16
increasing P concentration by 1 and 3 mg/L, the algal biomass reached
0.88 ± 0.06 and 0.94 ± 0.03 g/L, respectively, whereas only about
0.71 ± 0.02 g/L algae was obtained without extra P addition. In the
systems with 6 and 9 mg/L extra P, the algal growth rates was lower
than the systems with small dose of extra P and eventually yielded
biomass concentrations of 0.75 ± 0.03 and 0.62 ± 0.04 g/L. Previous
studies reported that higher phosphorus was beneficial for algae growth
(Chu et al., 2014; Roopnarain et al., 2014). However, the system with
the highest phosphorus concentration did not obtain the highest bio-
mass in this study.
Lower concentrations of trace metals like Mg and Fe were observed
in the catholyte of the system with 9 mg/L extra P. Less trace metals
may be one of the reasons that algal growth was limited when extra P
was 9 mg/L. The N/P (molar) ratio increased continuously in these
systems because the ammonium in the anodic chambers could con-
tinuously migrate through the CEM to the cathodic chambers. It could
be estimated that the N/P ratio in the control system exceeded 150, so
the algae in the control system was limited by P concentration (Arbib
et al., 2013).
3.1.2. Bioelectricity generation
The power generation from the MFC that has an algae-assisted
cathode was usually controlled by the dissolved oxygen (DO) produced
by algae (Campo et al., 2013). The systems with 6 mg/L extra P ob-
tained a maximal power density of about 2.8 W/m3 on the 2nd day
(Fig. 2b). However, the power density of this system decreased rapidly
in the following days, which was affected by the growth of algae. The
power density in the systems with 1 and 3 mg/L extra P showed similar
tendencies. The highest power densities of the two systems were about
2.6 W/m3, which occurred on the 2nd day, then decreased to about
1.2 W/m3 on the 8th day. Power densities in the systems with 1 and
3 mg/L extra P were raised again to about 1.7 W/m3 on the 10th day,
which was obviously higher than in the systems with higher P con-
centrated.
Previous study reported that the highest power density obtained
using a MFC with rectangular chambers to produce bioelectricity from
digested food waste was about 0.7 W/m3 (Li et al., 2013a). The higher
power density observed in the present study may be due to the con-
figurations of the tubular PMFC, which has a low internal resistance,
achieved through reducing the electrodes spacing and avoiding ohmic
loss in the cathodic electrolytes. Additionally, the large area of CEM
was beneficial for the charge and pH neutrality between anodic and
cathodic chambers (Logan et al., 2006).
H. Pei et al. Bioresource Technology 256 (2018) 11–16

Table 1 proteins were the dominant organic species in the ADE-KW (Fig. 3). The
Energy production in systems with different amounts of added phosphorus (P) in the intensities of both Peak A and Peak B reduced dramatically, revealing
catholyte.
that soluble microbial byproduct-like material and aromatic proteins
Extra P Lipid content Energy production (kWh/m3-ADE-KW) could easily be removed by the PMFC.
concentration (%) It was observed Peak A and Peak B were blue-shifted in the ex-
(mg/L) Electricity Lipid Total perimental period. The emission wavelengths of Peak A decreased from
354 nm to 338 nm in the initial 8 days and emission wavelengths of
0 (Control) 40.2 ± 4.2 0.50 ± 0.07 3.16 ± 0.43 3.66 ± 0.49
1 35.5 ± 3.7 0.53 ± 0.06 3.51 ± 0.63 4.04 ± 0.71 Peak B decreased from 353 nm to 334 nm in the initial 12 days. Blue
3 33.7 ± 4.4 0.57 ± 0.08 3.56 ± 0.57 4.13 ± 0.65 shifts were related to a decomposition of condensed aromatic moieties
6 37.5 ± 1.0 0.57 ± 0.01 3.16 ± 0.21 3.73 ± 0.22 and break-up of the large molecules, such as a decrease in the number
9 39.1 ± 2.6 0.48 ± 0.06 2.74 ± 0.36 3.22 ± 0.42 of aromatic rings, a reduction of conjugated bonds or an elimination of
particular functional groups (Wang et al., 2009). Thus, these shifts
demonstrated that the soluble microbial byproduct-like material (Peak
3.1.3. Bioenergy production
A) and the aromatic proteins (Peak B) from ADE-KW were degradable,
Algae are one of the promising feedstocks for biodiesel production.
and indeed they were degraded in the early stage of the experiment.
The lipid contents of the algae are shown in Table 1. Higher lipid
However, the intensity of Peak A decreased slowly whereas Peak B
content of the algae was observed in the control systems, which yielded
decreased rapidly in the initial 8 days, which may be attributed to the
the low biomass productivity. The energy that produced from lipid
aromatic proteins substances being more preferentially degraded than
accounted for about 86% of the total energy produced by the whole
soluble microbial byproduct-like material.
system. The electricity produced in the systems with 3 mg/L and 6 mg/L
Fulvic acid-like substances could also be degraded in the PFMC,
extra P was about 0.57 kWh/m3-ADE-KW, which was higher than other
whereas the removal rate was relatively lower than soluble microbial
systems. The maximal energy of 4.13 kWh/m3-ADE-KW was produced
byproduct-like material and aromatic proteins. Peak D (emission/ex-
when the P concentration was 3.7 mg/L. Excessive P not only reduced
citation wavelengths 476/415 nm) were related to the humic acid-like
the energy in the form of algae lipid but also reduced the bioelectricity.
organics. The intensity of Peak D reduced rapidly and the peak dis-
appeared on the 8th day. The humic substances are refractory and
3.2. Organics removal and mechanisms
constitute a component of organic matter (Chen et al., 2003). Previous
studies have demonstrated that the hydrophobic humic acid-like com-
3.2.1. Removal of organics in different systems
pounds were not easily degraded by the microbes in the MFC (Li et al.,
The fuel cell systems were fed with ADE-KW that contained high
2016). The substances located at Peak D may be different from the
concentrations of residual organics, with about 4530 ± 108 mg/L
hydrophobic humic acid-like organics, and they were preferentially
COD. The performance of the PMFC regarding COD removal is shown in
degraded by the PMFC system.
Table 2. About 78.1% of the COD was removed when the P con-
Large-molecular organics are less degradable in the bioelec-
centration was boosted by 3 mg/L, which delivered the highest bioe-
trochemical system (Li et al., 2013a). The blue shifts at Peak A and Peak
lectricity production. The systems with the highest P concentration
B indicated that the organics with large molecular were likely decom-
(extra P = 9 mg/L) in the catholyte corresponded to the least COD re-
posed into small-molecular organics through diverse metabolisms such
moval (64.9%). About 68.8% of the COD was removed when there was
as fermentation process. Then the organics with lower molecular, such
no extra P addition. It was observed that the systems which were not
as soluble sugar, protein or fatty acids, were degraded rapidly in the test
suited for algal growth yielded low COD removal efficiencies. The
systems, while the recalcitrant groups were resistant to biodegradation.
average Coulombic efficiency of these systems was about 17.2%, which
The substrate consumption via fermentation process might explain the
is similar to results from other studies using complex substrates
relatively low CE in the systems.
(Fornero et al., 2010). Some competing metabolic processes, such as
fermentation and methanogenesis among these complex substrates in
the anolyte might decrease the CE (Pant et al., 2010).
3.3. Nitrogen transportation and removal

3.2.2. Mechanism of organics removal in the PMFC

3.3.1. Nitrogen removal in different systems
The EEMs of the system with 3 mg/L extra P were shown in Fig. 3.
Nearly all of the nitrogen in the ADE-KW was in the form of am-
Four main peaks could be identified from the fluorescence spectra of
monium (99%). Compared to the traditional MFC systems, the PMFC
the ADE-KW. Peak A was associated with soluble microbial byproduct-
systems showed a better ability to remove ammonium, because am-
like material (chiefly tryptophan & protein-like substances). Peak B was
monium could migrate from the anodic chamber to the cathodic
correlated with aromatic proteins. Peak C was related to fulvic acid-like
chamber and then be assimilated by algae or removed through si-
substances. Peak D was described as humic acid-like organics (Zhou
multaneous nitrification and denitrification. The ammonium removal in
et al., 2013).
the anodic chambers is shown in Fig. 4a. About 79.0% of the 1550 mg/L
The high fluorescence intensities at Peak A and Peak B demon-
ammonium was removed in the anodic chamber in the system when
strated that soluble microbial byproduct-like material and aromatic
there was 3 mg/L extra P, whereas only 67.8% of the ammonium was
removed in the system when there was 9 mg/L extra P.
Table 2
COD removal in the anodic chamber and Coulombic efficiency of the PMFC with different
The increasing of ammonium concentration in the cathodic cham-
amounts of added phosphorus (P) in the catholyte. bers was shown in Fig. 4a. The ammonium concentration in the system
with 3 mg/L extra P increased from 47.6 mg/L to 85.8 mg/L, whereas
Extra P Effluent COD (mg/L) Removal Coulombic the system with 9 mg/L extra P even increased by a factor of about 2.4
concentration (mg/ efficiency (%) efficiency (%)
(112 mg/L). In terms of the whole system, 59.8% of the nitrogen was
L)
removed in the system with 3 mg/L extra P, whereas only 44.1% of the
0 (Control) 1413.3 ± 73.2 68.8 ± 1.6 17.9 nitrogen was removed in the system with 9 mg/L extra P (Table 3).
1 1105.1 ± 34.7 75.6 ± 0.8 16.7 Hence, the system that was beneficial for algae growth also obtained
3 993.5 ± 154.0 78.1 ± 3.4 16.6
high nitrogen removal efficiency, since the algae can not only assimilate
6 1174.7 ± 104.0 74.1 ± 2.3 17.5
9 1590.1 ± 84.2 64.9 ± 1.9 17.3 ammonium by themselves but also provide O2 for ammonium oxidi-
zation.

14
H. Pei et al. Bioresource Technology 256 (2018) 11–16

Fig. 3. Fluorescence EEMs of ADE-KW during organic degradation in the system in which additional phosphorus concentration was 3 mg/L. (For interpretation of the references to colour
in this figure legend, the reader is referred to the web version of this article.)

3.3.2. The mechanism of nitrogen removal in the PMFC
The nitrate and nitrite concentration in these anodic chambers re-
mained below the detection limit, which means that nitrification in the
anodic chamber could be ignored (Fig. 4b and c). Only 2–6% aqueous
ammonium was in the form of NH3 at the pH (about 7.5–8.1) of the
anolyte (Emerson et al., 1975). In addition, the PMFC was a closed
system, so ammonia evaporation only accounted for a small part of
nitrogen removal. It was notable that the ammonium decreased rapidly
in the anolyte with the increase of ammonium in the catholyte. Am-
monium migration for charge neutrality and diffusion due to con-
centration gradient were the main driving force for ammonium transfer
from the anodic chamber to the cathodic chamber (Haddadi et al.,
2013). It was estimated that the ammonium transport to meet charge
neutrality accounted for about 31% of the Coulombs. The ammonium
transportation rate in these system ranged from 2.3 to 2.7 g/(m2·d),
which were smaller than the transportation rate of 8.5 g/(m2·d) ob-
served in a previous study that had a higher ammonium concentration
(Table 3) (Haddadi et al., 2013).
The nitrogen in the catholyte could be removed as an electron ac-
ceptor or assimilated by algae. The nitrogen mass fraction of the dry
algal biomass was determined in order to quantify the nitrogen as-
similated by algae. The results indicated that only 9.1%–14.6% of the

Fig. 4. Concentrations of NH4+-N (a), NO2−-N (b) and NO3−-N (c) in the anolyte and catholyte of the systems with different extra phosphorus levels in the catholyte. (d) is simplified
schematics of nitrogen elimination in the systems for the system with extra P = 3 mg/L.

15
H. Pei et al.
Table 3
Ammonium transportation rate from the anodic chamber to the cathodic chamber and
nitrogen removal in systems with different amounts of added phosphorus (P) in the
catholyte.
Extra P NH4+ Overall Overall nitrogen
concentration transportation rate nitrogen accumulated in algal
(mg/L) (g/(m2·d)) removal (%) biomass (%)
0 (Control) 2.47 49.1 10.6
1 2.61 56.3 13.5
3 2.69 59.8 14.6
6 2.45 49.4 11.6
9 2.30 44.1 9.1
overall nitrogen (the whole system) was accumulated by algae, and the
average nitrogen assimilation rate by algae was about 2.5 mg/(L·d),
consistent with the previously reported figures of between 0.5 and
12 mg/(L·d) (Marcilhac et al., 2014).
Algae preferred to assimilate ammonium rather than nitrate or ni-
trite because nitrogen is ultimately reduced to ammonium before being
incorporated into amino acids within the intracellular fluid (Cai et al.,
2013). Therefore, the accumulation of nitrate and nitrite in the system
demonstrated that some nitrogen was removed as electron acceptors at
the cathode. Both nitrate and nitrite could be used as electron acceptors
for current generation, albeit at lower levels than for oxygen (Virdis
et al., 2010). Current production relies on the reduction of oxygen in
the absence of ammonium. Whilst upon ammonium injection, O2 is
utilized by nitrifiers that grow on the surface of the cathode, limiting O2
penetration into the biofilm as an electron acceptor. In that case, cur-
rent is mainly affected by the reduction of the nitrate or nitrite (Virdis
et al., 2010). In this study, as the ammonium was excess in the cathodic
chamber, the higher the dissolved oxygen concentration was, the more
nitrate and nitrite were removed as electron acceptors.
Considering all trials performed in this study, a strong relation be-
tween nitrogen removal rate and dissolved oxygen indicated that most
of the nitrogen removal was related to ammonium oxidation. Because
of the presence of excess ammonium, the majority of the nitrification
products, namely nitrate and nitrite, would be eliminated due to
cathodic denitrification instead of being accumulated by algae.
Therefore, ammonium was removed mainly as electron acceptors at the
cathode after being oxidized to nitrification products by oxygen.
4. Conclusion
An extra P concentration of 3 mg/L was optimal for the tubular
PMFC in this study. Soluble microbial byproduct-like material and
aromatic proteins were the dominant organics in the ADE-KW, which
were also readily degradable in PMFC system. Ammonium was re-
moved mainly as electricity acceptors at the cathode after being oxi-
dized by oxygen, whereas algal assimilation only accounted for about
14.6% of the overall nitrogen. Further study could be conducted to
improve the performance of the tubular PMFC according to the algal
growth characteristics.
Acknowledgement
This research was funded by: National Science Fund for Excellent
Young Scholars (51322811); Science and Technology Development
Planning of Shandong Province (2012GGE27027); Program for New
Century Excellent Talents in University of Ministry of Education of
China (Grant NO. NCET-12-0341); and Foundation for Outstanding
Young Scientists in Shandong Province (ZR2016EEB26).
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in the
16
Bioresource Technology 256 (2018) 11–16
online version, at http://dx.doi.org/10.1016/j.biortech.2018.01.144.
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