Science of the Total Environment 907 (2024) 167827

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Science of the Total Environment

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

Performance analysis of microbial fuel cell - membrane bioreactor with

reduced graphene oxide enhanced polypyrrole conductive ceramic
membrane: Wastewater treatment, membrane fouling and microbial
community under high salinity
Rui Wang a, Hong You a, b, Binghan Xie a, b, Guoyu Zhang a, b, Jing Zhu a, b, *, Weirun Li a,
Xinan Dong b, Qiqing Qin b, Mengying Wang a, Yi Ding c, Haili Tan b, Yuhong Jia b,
Zhipeng Li a, b, *
a
State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China
b
School of Marine Science and Technology, Harbin Institute of Technology at Weihai, Weihai 264209, China
c
Marine College, Shandong University, Weihai 264209, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• A novel MFC-MBR with rGO enhanced

PPy conductive ceramic membrane was
developed.
• Over 90 % for TOC and 86 % for NH+ 4 -N
removal efficiencies were obtained in
MFC-MBRs.
• Electric field improved the abundance of
dominant microbial communities and
genes.
• rGO/PPy membrane with superior con­
ductivity strengthened performances of
MFC-MBR.

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

Editor: Huu Hao Ngo The application of membrane bioreactor (MBR) in high salinity wastewater treatment was mainly hindered by
membrane fouling. Microbial fuel cell (MFC)-MBR coupling system was established to alleviate membrane
Keywords: fouling and save energy. Reduced graphene oxide/polypyrrole ceramic membrane (rGO/PPy CM) with high
MFC-MBR conductivity and stability was innovatively placed in MFC-MBRs as both cathode and filter, with PPy CM, rGO/
rGO/PPy conductive ceramic membrane
PPy CM and CM placed in other reactors. MFC-MBR (rGO/PPy) and MFC-MBR (PPy) achieved higher pollutant
Membrane fouling
removal efficiencies (90.73 % and 90.45 % for TOC, 87.22 % and 86.56 % for NH+ 4 -N, respectively) and superior
Microbial community analysis
High salinity wastewater anti-fouling performance (1.86 and 1.93 kPa/d for average membrane fouling rates) than both conventional
MBRs (CMBRs). The stable voltage generation was around 287 and 242 mV, respectively. Through high
throughput sequencing, electric field showed a positive correlation with the abundance and activity of most
dominant phylum (Bacteroidetes, Chloroflexi, Actinobacteria, and Firmicutes) and functional genes (amoA, hao,
narG, napA, nirK, norB, and nosZ), thereby improving pollutant removal efficiency. The higher conductivity of
rGO/PPy CM resulted in enhanced electric field intensity, leading to superior performance of anti-fouling and

* Corresponding authors at: School of Marine Science and Technology, Harbin Institute of Technology at Weihai, Weihai 264209, China.
E-mail addresses: zhujing@hit.edu.cn (J. Zhu), lizhipengcn@hit.edu.cn (Z. Li).

https://doi.org/10.1016/j.scitotenv.2023.167827
Received 13 August 2023; Received in revised form 3 October 2023; Accepted 12 October 2023
Available online 13 October 2023
0048-9697/© 2023 Published by Elsevier B.V.
R. Wang et al.
pollutant removal. This study inventively explored the effects of conductive membrane property on electricity
generation performance, microbial community, pollutant removal and membrane fouling, providing theoretical
support for the selection of electrode materials in MFC-MBR.
1. Introduction
Mariculture wastewater, as a typical high saline wastewater, can
cause osmotic stress and increase ion toxicity, leading to cell cyto­
plasmic lysis and microbial death. Nitrogen-containing mariculture
wastewater is generally considered difficult to treat, whose direct
discharge will lead to acidification and eutrophication of the coastal
marine ecosystem, thereby endangering aquatic life (Zhu et al., 2020;
Zhu et al., 2022). In recent years, membrane bioreactors (MBRs),
combining biological treatment and membrane filtration, have been
widely used in the treatment of high saline wastewater due to their
unique advantages such as high effluent quality, low sludge production
and small footprint (Chen et al., 2019; Song et al., 2020b; Zhang and
Jiang, 2019). However, foulants inevitably adsorb on the membrane
surface and pore walls during operation of MBRs, leading to membrane
fouling and limiting the widespread use of MBRs (Zhang et al., 2022;
Zhang et al., 2021). As the main pollutants in MBR, such as soluble
microbial products (SMP) and extracellular polymers (EPS), are often
negatively charged, the use of electric field to control membrane fouling
is receiving extensive attention (Hawari et al., 2015; Yin et al., 2020).
Actually, the high salinity in mariculture wastewater can further
enhance the effectiveness of electric field MBR, as it acts as a conductive
medium that facilitates the electrochemical decomposition and precip­
itation of organic and particulate pollutants (Jiang et al., 2022).
However, this method involves high energy consumption, and bac­
teria may become inactive under high electric fields (Xue et al., 2016).
Generally, DC density higher than 2.5 A/m2 can affect microbial activity
by reducing the activity and/or growth rate of nitrifying bacteria
(Ensano et al., 2016). At the same time, high-density current can lead to
an increase in the production of pollutants such as SMP, which can affect
the performance of MBR with electric field (Zhang et al., 2015). How­
ever, applying a low electrical intensity is beneficial to the growth of
bacteria. For example, a current density of 200– 250 mA/m2 can stim­
ulate the growth of denitrifying bacteria, which are responsible for the
complete removal of nitrite nitrogen (Liu et al., 2015). Therefore, the
selection of current intensity (voltage) is crucial. In addition, wastewater
recovery and reuse are crucial for avoiding water scarcity and envi­
ronmental degradation. Sustainable and low-energy consumption tech­
nologies are particularly important for achieving these goals (Malaeb
et al., 2013). Fortunately, microbial fuel cell (MFC) is considered as a
promising renewable energy wastewater treatment technology, which
generates electricity through microbial oxidation/pollutants meta­
bolism that release electrons to the anode (Logan et al., 2006). While,
due to the poor quality of effluent in MFC, post-treatment is usually
required to meet the effluent discharge standards (Wang et al., 2015). To
reduce the energy consumption of MBR with external electric field and
improve the effluent quality of MFC, researchers have proposed an in­
tegrated technology of MFC and MBR.
There are two methods for this assembly technology: one is to place a
non-conductive membrane between the two electrodes of the MFC, and
the other is to use a conductive membrane as the cathode of MFC.
Studies have shown that the latter can lead to a higher interest owing to
its ability to augment the efficacy and spatial utilization of the electric
repulsion effect (Wang et al., 2023a; Yang et al., 2019). While, there are
few low-cost options commercially available, with carbon and metal
membranes being expensive. Considering the favorable properties of
ceramic membranes (CM) like remarkable mechanical stability and
strength, it is imperative to contemplate incorporating a cost-effective
and highly conductive layer onto the ceramic membrane. Polypyrrole
(PPy) has emerged as a leading conductive polymer due to its
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Science of the Total Environment 907 (2024) 167827
exceptional features such as robust stability, strong electrical conduc­
tivity, and ease of synthesis (Liu et al., 2012b). Furthermore, by incor­
porating reduced graphene oxide (rGO), the active sites and surface area
of PPy can be increased, thereby enhancing penetration performance
and electrical conductivity through the inherent conductivity of rGO
(Jiang et al., 2020b; Liu et al., 2013). In our previous study, PPy CM and
rGO/PPy CM with excellent and stable conductivity were prepared and
verified that they could form a barrier around the membrane through
electrochemical repulsion under an external electric field, thus pre­
venting negatively charged pollutants from adhering to the membrane
surface (Wang et al., 2023b). The excellent potential of the conductive
membranes under electric field suggested its applicability in MFC-MBR.
In light of the energy characteristics of MFC, the presence of mi­
croorganisms that are capable of generating and transferring electrons
outside the cell is crucial for effective electricity generation (Kumar
et al., 2015; Logan, 2009). Most studies focused on the performance of
conductive membrane for energy production and pollutant removal in
MBR-MFC (Li et al., 2019b; Li et al., 2017; Malaeb et al., 2013). Some
studies reported microbial metabolic pathways in coupled systems. For
example, Pierangeli et al. found that the microbial community formed in
the electron beam could degrade organic matter and remove toxic
compounds (such as aromatic compounds) and nitrogen, while gener­
ating energy in MBR-MFC (Fonseca Pierangeli et al., 2021). However,
there is little research about the effects of electric field intensity on
microbial abundance and metabolic pathways from the perspective of
the electrode or conductive membranes, especially for mariculture
wastewater treatment. Therefore, the conductive ceramic membrane
modified by PPy and rGO was developed and firstly applied in MFC-MBR
for mariculture wastewater treatment, aiming to provide guidance on
enhancing the performances of MFC and MBR.
In this study, four reactors were utilized to treat artificially simulated
mariculture wastewater, where PPy CM and rGO/PPy CM were sepa­
rately integrated into MFC-MBRs, labeled as MFC-MBR (PPy) and MFC-
MBR (rGO/PPy) to investigate the impact of electrodes on the electro­
chemical and wastewater treatment performances. CM support and
rGO/PPy CM were implemented in MBRs without electric field as con­
trol groups, namely CMBR (CM) and CMBR (rGO/PPy). The main ob­
jectives of the study were to: 1) analyze the performance of the four
MBRs, including wastewater treatment efficiency and membrane
fouling; 2) investigate the electricity generation performance of two
MFC-MBRs; 3) explore the anti-fouling and pollutant removal mecha­
nism of MFC-MBR based on microbial community analysis and func­
tional gene prediction.
2. Materials and methods
2.1. Construction and operation of MFC-MBR system
The preparation methods of PPy CM and rGO/PPy CM can be found
in previous study (Wang et al., 2022). The properties of the two
conductive membranes and CM support are shown in Table S1. The
traditional MBRs utilizing CM support and rGO/PPy CM were used as
control groups, MFC-MBRs with PPy CM and rGO/PPy CM were
designed and constructed as experimental groups. Fig. 1 was the sche­
matic diagram of the MFC-MBR system. The coupling system consisted
of a cathode chamber and an anode chamber without proton-exchange
membrane. The anode adopted a carbon brush, which was centered on
two titanium wires and fixed by spiral rotation. The overall size of
carbon brush was 30 mm × 100 mm, and it was two carbon brushes that
were arranged in parallel to facilitate the attachment of microorganisms.
R. Wang et al. Science of the Total Environment 907 (2024) 167827

The cathode of the reactor was a conductive membrane component, was the internal resistance of the system (Wang et al., 2020). The po­
which was composed of two ceramic conductive membranes fixed by a larization curve and power density curve could intuitively reflect the
porous organic partition. The conductive membrane coupled MFC-MBR power generation capacity of system, which were important means to
system mainly consisted of an external resistance box, an influent and study the mechanism of electrode processes. The current and anode
effluent tank, a vacuum meter, and a reactor. The resistance size of the power density were obtained from Eqs. (1) and (2) (Gao et al., 2017):
external resistance box was set to 1000 Ω, the volumes of the coupling
I = U/R (1)
system anode and cathode chamber were 130 mL and 368 mL,
respectively.
P = UI/V (2)
The influent of the system was artificially simulated mariculture
wastewater. Related chemical reagents (Table S2) were added to the where, R was the external resistance. U and I were the voltage (V) and
seawater (Weihai) as microbial carbon source, nitrogen source and other current value (A) measured under the external resistance loaded,
nutrients, so that the system could operate stably and continuously. The respectively. V was the volume of the anode chamber (m3). P was the
sludge used in the reactor was aerobic sludge from Weihai Third Sewage anode power density of the system, W/m3.
Treatment Plant, which was acclimated with seawater and inoculated
into reactors. That was, by gradually increasing the proportion of
2.3. High throughput sequencing
seawater in the inlet (from 0 to 100 %), the power-generating micro­
organisms in the system were gradually domesticated, enabling the
To investigate the effects of self-generated electric field and electrode
growth of halophilic power-generating microorganisms in high salt en­
materials on bacterial communities, bacterial primer 338F_ 806R was
vironments. The inlet was continuously pumped from the bottom of the
used for the V3-V4 region of the 16S rRNA gene, which was amplified by
anode chamber by the peristaltic pump (Lange, China). After the water
Polymerase chain reaction (PCR) on the TransStart Fastpfu DNA Poly­
entered the cathode chamber through the baffle plate, it was pumped
merase system with PCR instrument (ABI GeneAmp® Type 9700).
out by the membrane module and pump. The baffle plate spacing was set
Subsequently, high-throughput sequencing was performed on the MiSeq
at 8 mm. The four MBR reactors were operated under constant flux
PE platform (Illumina, USA) of Majorbio Bio Pharm Technology Co., Ltd.
conditions (8 L⋅m− 2⋅h− 1), with the suction pump following an inter­
(Shanghai, China) based on the Silva database.
mittent operation mode (running for 8 min, then stopping for 2 min).
In order to understand the nitrogen metabolic pathways in CMBR
The MLSS in all MBRs remained between 3500 and 4000 mg/L, with pH
and MFC-MBR, the functional composition of microbial communities in
ranging from 6.52 to 8.12, and operated at room temperature. The TMP
the samples from amplicon sequencing results was predicted (PIC­
of the membrane module was monitored by a vacuum gauge set between
RUSt2), and the protein sequences of the predicted genes were
the membrane module and the peristaltic pump. During the operation of
compared using the Kyoto Encyclopedia of Genes and Genomes (KEGG)
the four MBRs, when the TMP of the cathode membrane reached 0.04
database. Functional genes related to nitrogen metabolism were iden­
MPa, the systems were paused and the membrane components were
tified based on protein sequence prediction (Caicedo et al., 2020).
cleaned before restarting.

2.4. Chemical analysis and characterization

2.2. Electrochemical test
A multimeter (Tianyu, China) was connected to the external circuit
of the system, whose voltage between the positive and negative poles of
the system was measured every 24 h. During stable operation of MFC,
open circuit operation was exceeded 4 h. Then the power density and
polarization curve under different external resistance values were
measured. The external resistor was firstly disconnected before testing,
then the multimeter was connected to monitor the open circuit voltage.
The resistance box was connected to the entire circuit after the multi­
meter indicator becoming stable. Then the multimeter measured the
voltage of the external resistor. After continuously changing the external
resistance from small to large (10.0– 99,999.9 Ω), the current was
calculated based on the corresponding resistance and voltage (Li et al.,
2019b). By recording the voltage obtained at each resistor, the current
was calculated and polarization curve was drawn. The slope of the curve
The main analysis of the sewage treatment effect was the removal
efficiencies of TOC and NH+ 4 -N. Before testing TOC, water sample was
filtered with filter membrane (Haiyan New Oriental Plastic Technology
Co., Ltd., 0.45 μM), diluted, then measured by TOC analyzer (Shimadzu,
Japan). NH+ 4 -N was measured with UV–vis spectrophotometer (Puxi,
China) by Nessler's reagent UV spectrophotometry. Scanning electron
microscopy (SEM, Zeiss, England) was used to analyze the surface
morphology of the membranes and carbon brush.
3. Results and discussion
3.1. Wastewater treatment performance and membrane fouling
As shown in Fig. 2 (A), the average influent concentration of TOC
was 259.62 mg/L. MFC-MBR (PPy) (90.45 %) and MFC-MBR (rGO/PPy)

Fig. 1. Schematic diagram of (A) MFC-MBR system and (B) membrane module.

3
R. Wang et al.
Fig. 2. The variation of (A) TOC; (B) NH+
4 -N; (C) TMP; (D) SEM images in four reactors.
(90.73 %) had superior removal efficiencies of TOC, followed by CMBR
(rGO/PPy) (88.38 %) and CMBR (CM) (87.71 %). As the operating
conditions (such as sludge concentration) in the four MBRs were the
same, the difference in pollutant removal efficiencies was mainly
determined by membranes types and electric field. The above result
showed that moderate voltage was beneficial for the removal of TOC,
which was consistent with the results of Ding et al. (2018) and Wang
et al. (2023b). Compared with MFC-MBR (PPy), the slight increase in
removal rate of TOC in MFC-MBR (rGO/PPy) might be attributed to the
enhancement of bacteria abundance related to organic degradation,
which could be influenced by variations in electric field.
From Fig. 2 (B), the average influent concentration of NH+ 4 -N was
18.12 mg/L. MFC-MBR (rGO/PPy) had the highest removal efficiency of
NH+ 4 -N (87.22 %), followed by MFC-MBR (PPy) (86.56 %), CMBR (rGO/
PPy) (82.01 %) and CMBR (CM) (80.64 %). It was worth noting that the
influence of microfiltration membranes on NH+ 4 -N removal was mini­
mal. Under self-generated electric field, electrochemical effects could
promote microbial metabolism and enhance metabolic activity for
nitrification and denitrification, thereby indirectly improving the
removal efficiency of NH+ 4 -N (Ding et al., 2016; Jiang et al., 2020a). The
removal efficiency of NH+ 4 -N in MFC-MBR (rGO/PPy) was higher than
that in MFC-MBR (PPy), which might be due to significant differences in
the abundance of denitrification related microorganisms caused by the
electric field difference. This would be further elaborated in the subse­
quent analysis of microbial communities.
Fig. 2 (C) was the curves of TMP during the operation in four re­
actors, whose average membrane fouling rates were 2.5 kPa/d (CMBR
(rGO/PPy)), 2.2 kPa/d (CMBR (CM)), 1.93 kPa/d (MFC-MBR (PPy)) and
1.86 kPa/d (MFC-MBR (rGO/PPy)). This indicated that the growth rate
of membrane fouling was effectively slowed down in MFC-MBR system.
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Science of the Total Environment 907 (2024) 167827
Previous studies showed that the pollutants in MBR were mainly nega­
tively charged, leading to electrostatic repulsion between them when a
conductive membrane was used as the cathode. The electrostatic
repulsion increased with the increase of electric field intensity, resulting
in a stronger anti-adhesion ability of the membrane surface (Udomkit­
tayachai et al., 2021; Wang et al., 2023b). This elucidated the enhanced
anti-fouling performance was observed in MFC-MBR (rGO/PPy)
compared to MFC-MBR (PPy), due to its superior self-generated
potential.
After the reaction was completed, the morphologies of membrane
surface of four reactors were observed by SEM. From Fig. 2(D), both
CMBR systems had severe membrane pore blockage on the membrane
surface. However, there were more voids on the membrane surface of
the two MFC-MBRs, indicating that electric field could slow down the
deposition of foulants on the membrane surface, thereby alleviating
membrane fouling (Jiang et al., 2020a). Besides, the pores on the
membrane surface of MFC-MBR (rGO/PPy) were relatively larger than
that of MFC-MBR (PPy), which was consistent with the above conclusion
of superior anti-fouling performance in MFC-MBR (rGO/PPy).
3.2. Electrochemical performance of MFC-MBR
Multimeter was used to regularly monitor the voltage generated by
the coupling system. With a constant resistance of 1000 Ω, the potential
of the two MFC-MBR systems changed over time as shown in Fig. 3 (A).
In the initial stage of coupling system, the system potential was rela­
tively low, but increased rapidly. When the potential of MFC-MBR (PPy)
and MFC-MBR (rGO/PPy) systems increased to around 242 and 287 mV,
respectively, the systems became stable. Continuous supply of nutrients
would maintain the continuous transportation of solution and proton
R. Wang et al.
Fig. 3. (A) Changes in MFC-MBR output voltage over time; (B) Polarization curve and power density curve; (C) Linear fitting of polarization data; (D) The variation
of voltage and current with resistance; (E) Current density of cathode and anode of MFC-MBR (PPy) and MFC-MBR (rGO/PPy).
from anode to cathode (Wang et al., 2013), which also enabled good
growth of halophilic electrogenic microorganisms in high salt environ­
ment. Besides, a higher potential in MFC-MBR (rGO/PPy) would
generate a stronger electric field and electrostatic repulsion compared
with MFC-MBR (PPy).
After the output voltage stabilized, the power density curve and
polarization curve of the system were determined. As shown in Fig. 3
(B), the current and the output power density was zero in an open circuit
state. As the current density increased, the power density gradually
enlarged. With an external resistance of 500 Ω, the open circuit voltage
(OCV) of MFC-MBR (PPy) and MFC-MBR (rGO/PPy) were 115.4 and
138 mV, respectively. And the power density reached the maximum
values of 3.80 and 5.44 W/m3, respectively. Subsequently, the power
density gradually decreased as the external resistance decreased. This
should be attributed to the fact that under higher external resistance
conditions, it was more conducive to the reproduction of electricity
producing microorganisms on the anode, thereby increasing its power
output (Wang et al., 2013). This maximum power density was higher
than the 0.629 W/m3 measured by Zhou et al. in the overflow type
EMBR system (Zhou et al., 2015). It was also higher than the maximum
power densities obtained in MFC reported by Wang et al. (0.123 W/m3)
(Wang et al., 2013) and aerobic activated sludge systems reported by
Zhu et al.(0.037 W/m3) (Zhu et al., 2013).
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Science of the Total Environment 907 (2024) 167827
Linear fitting on the voltage-current polarization curve data of the
MFC-MBR system was performed, and the absolute value of the slope
obtained was the internal resistance value of the system (Fig. 3(C)). The
linear slopes of the MFC-MBR (PPy) and MFC-MBR (rGO/PPy) curves
after linear fitting were − 481.37 and − 458 Ω, respectively, that was,
the internal resistances were 481.37 and 458 Ω, respectively. From the
configuration diagram of the system, an aeration system was installed at
the bottom of the cathode. The aeration system not only provided suf­
ficient oxygen for MBR, but also kept the sludge mixture in a disturbed
state. The disturbance of fluid could effectively promote the transfer
efficiency of H+ between the anode and cathode, thereby reducing the
internal resistance of the battery. In short, MFC-MBR (rGO/PPy) in this
study could maintain a smaller internal resistance and stronger power
generation capacity compared with MFC-MBR (PPy).
Fig. 3 (D) shows the changes in voltage at both ends of the resistor
and system current when the external resistance increased. During the
process of increasing the external resistance from 20 Ω to 10,000 Ω, the
voltage changed rapidly with the resistance value. MFC-MBR (PPy)
quickly increased from 5.8 mV to 252.4 mV, and MFC-MBR (rGO/PPy)
quickly increased from 8 mV to 311 mV. Afterwards, the resistance
enlarged from 10,000 Ω to 99,999.9 Ω, the voltage increased slowly.
When it reached 20,000 Ω, the voltage stabilized and remained almost
unchanged, with the highest point voltages of 270 and 338 mV,
R. Wang et al.
respectively. At the same time, the current showed a decreasing trend as
the external resistance increased. The initial current of MFC-MBR (PPy)
and MFC-MBR (rGO/PPy) were 0.58 and 0.8 mA, respectively. Similar to
the change in voltage, the decrease rates of current were very fast in the
early stage. After the external resistance reached 20,000 Ω, the current
remained almost close to zero in both MFC- MBRs.
Fig. 3 (E) shows the current densities of the cathode and anode of two
MFC-MBRs. The effective filtration area of the cathode was 22.68 cm2,
and the effective volume of the anode was 7 cm3. The maximum current
densities of the cathode and anode of MFC-MBR (PPy) could reach
255.73 mA/m2 and 82.86 mA/m3, respectively. For MFC-MBR (rGO/
PPy), it could reach 352.74 mA/m2 and 114.29 mA/m3, respectively.
Therefore, with PPy and rGO/PPy conductive membranes as cathodes,
the continuous flow of water from the anode chamber to the cathode
chamber could achieve high stability of power generation and high
voltage output in the system, thereby efficiently generating electricity
from wastewater. In general, MBR-MFC(rGO/PPy) with highly
conductive cathode membrane reinforced by adding rGO could achieve
superior electricity generation, as well as electric field intensity, which
would be further analyzed in the later microbial community.
SEM was utilized to observe the microstructure on the surface of
carbon brush before and after use. From Fig.S1, a large number of mi­
croorganisms were attached to the surface of the carbon fiber filaments
in both reactors. The bacterial bodies were directly contacted or con­
nected by extracellular polymers, forming biofilm and wrapping it on
the surface of the carbon fiber filaments, which were mainly bacillus.
3.3. Microbial community analysis
3.3.1. Microbial abundance and diversity
Microorganisms play a crucial role in the treatment of mariculture
wastewater, whose community structure and synergistic mechanisms
have a significant impact on the electricity production performance of
MFC. In order to investigate the effects of electric field and different
electrode materials on microbial communities, microorganisms from
inoculated activated sludge (control), conventional MBR (CMBR (rGO/
PPy)), as well as anodes of MFC-MBR (PPy) and MFC-MBR (rGO/PPy)
were sampled during stable operation period. As listed in Table 1, the
coverage of samples in each system exceeded 0.99, indicating that the
obtained data could reflect the true diversity of bacterial community in
samples.
The constructed dilution curve is shown in Fig. 4 (A). The curves of
all samples eventually tended to flatten, indicating that the sequencing
depth basically covered all species in samples. ACE index and Chao1
index were used to represent the index of community abundance, which
were positively correlated with the total number of representative spe­
cies (Choi et al., 2017). From Table 1, the ACE index and Chao1 index
were the highest in MFC-MBR (rGO/PPy), followed by MFC-MBR(PPy),
CMBR(CM) and inoculated sludge. This indicated that the microbial
community structure in different MBRs changed with the increase of
time, which was mainly affected by operating conditions (Chen et al.,
2020). The self-generated electric field would enhance species
Table 1
Microbial community analysis based on OUT level for microbial sequencing.
Sample ACE Chao Coverage Shannon Simpson Sobs
CMBR
1033.349 1018.889 0.993 4.212 0.079 864
(CM)
MFC-
MBR 1141.772 1124.497 0.992 4.728 0.029 950
(PPy)
MFC-
MBR
1128.438 1115.218 0.995 5.200 0.018 1008
(rGO/
PPy)
Control 771.349 770.718 0.996 4.446 0.045 669
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Science of the Total Environment 907 (2024) 167827
abundance. Both Shannon index and Simpson index were the diversity
index of microorganisms in the estimated sample. Microbial diversity
was positively correlated with Shannon index and negatively correlated
with Simpson index (Liu et al., 2017). Compared with inoculated sludge,
CMBR had a lower Shannon index and a higher Simpson index, indi­
cating a decrease in the diversity and uniformity of microbial commu­
nities in the CMBR system. This might be due to some microorganisms
being unable to adapt to the reaction environment and being eliminated
in competition with dominant bacteria. However, the two MFC-MBR
reactors had higher Shannon index and lower Simpson index, indi­
cating that the coupling system improved the diversity and uniformity of
microbial communities. Higher microbial diversity could promote more
effective power density generation and biomass utilization, especially
when there were more diverse electrically active microbial communities
in MFC (Song et al., 2020a).
Fig. 4 (B) shows the Veen plots of four samples, from which the
differences in microbial numbers between different samples could be
clearly observed. Among the four microbial communities, 206 OTUs
were shared by the four communities, accounting for 38 % of the total
OTUs, which were the microbial community that constituted the main
body of sludge. The number of overlapping OTUs between inoculated
sludge and sludge samples in CMBR (rGO/PPy), MFC-MBR (PPy), and
MFC-MBR (rGO/PPy) were 242, 275, and 280, respectively. The changes
in the number of microorganisms in the activated sludge samples were
more significant under electric field.
To investigate whether the biological electric field had altered the
structure of the microbial community within the coupled system, Prin­
cipal Component Analysis (PCA) was conducted. The more similar the
composition of the sample species, the closer the distance reflected in
the PCA diagram. From Fig. 4(C), the distance between the microor­
ganisms in the inoculated sludge and CMBR system was relatively far at
the PC2 level. However, the separation distance between the microor­
ganisms in two MFC-MBRs and inoculated sludge were relatively large
at the PC1 and PC2 levels, especially at the PC1 level. This indicated that
the phylogenetic relationship between the microorganisms in the two
systems was relatively far, indicating that the presence of a biological
electric field significantly changed the structure of the microbial (Fon­
seca Pierangeli et al., 2021).
3.3.2. Composition of microbial community structure
The microbial community would gradually undergo community
succession in response to changes in the environment. The relative
abundance of inoculated sludge and microorganisms in the three re­
actors is shown in Fig. 5. From the phylum level, Proteobacteria (30.12–
60.35 %), Bacteroidota (10.90– 18.00 %), Actinobacteriota (6.43–
28.53 %), Chloroflexi (2.32– 9.44 %) and Firmicutes (0.81– 5.22 %)
were widely found in the four samples. These bacteria were the domi­
nant bacteria in the activated sludge system, as well as in the marine
environment (Chen et al., 2017; Nancharaiah et al., 2018; Wu et al.,
2018). The abundance of Proteobacteria in CMBR (CM) (60.35 %) was
higher than that of MFC-MBR (PPy) (30.12 %) and MFC-MBR (rGO/PPy)
(34.7 %). As proteobacteria could secrete a large amount of EPS (Chu
et al., 2015), the decrease in abundance of Proteobacteria helped to
reduce EPS production. This was consistent with the previously
conclusion that the SMP and EPS contents in electric field MBR were less
than those in MBR without electric field (Wang et al., 2023b; Yin et al.,
2020).
The proportion of Bacteroidetes in inoculated sludge was 17.4 %,
higher than CMBR (CM) (10.9 %), MFC-MBR (PPy) (11.16 %) and lower
than MFC-MBR (rGO/PPy) (18.00 %), reflecting a positive correlation
with the intensity of the electric field. Bacteroidota was a known
fermentation bacteria and considered the most common phylum
responsible for effectively removing nitrogen and carbon (Meng et al.,
2017; Wu et al., 2018), which was also consistent with the previous
conclusion that higher electric field led to enhanced removal of TOC and
NH+4 -N. Similar to the trend of abundance change in Bacteroidetes, the
R. Wang et al.
Fig. 4. (A) Dilution curve; (B) Veen diagram; (C) PCA diagram of four samples.
relative abundance of Chloroflexi decreased from 9.44 % (inoculated
sludge) to 2.32 % (CMBR (CM)). However, its abundance increased to
4.44 % (MFC-MBR (PPy)) and 4.66 % (MFC-MBR (rGO/PPy)) under
electric field. Chloroflexi was a typical filamentous bacteria that was
often seen in the process of aerobic treatment (Bjornsson et al., 2002),
which could degrade EPS and SMP by secreting extracellular enzymes
(Han et al., 2021). The higher abundance of Bacteroidetes and Chloro­
flexi in MFC-MBR (rGO/PPy) compared to MFC-MBR (PPy) suggested
that a stronger electric field might be more conducive to their survival,
resulting in higher removal efficiency of nitrogen and carbon.
The abundance of Actinobacteria in inoculated sludge (6.43 %) and
CMBR(CM) (6.91 %) were similar. However, its abundance greatly
increased under electric field (28.53 % for MFC-MBR(PPy) and 17.37 %
for MFC-MBR(rGO/PPy)). Actinobacteria was filamentous bacteria
known for their ability to degrade metabolites and toxic compounds (Li
et al., 2019a; Zhang et al., 2012). Liu et al. showed that micro electric
field had a positive impact on the growth of filamentous bacteria (Liu
et al., 2012a). Besides, Mycobacterium and Propionibacterium, as
members of Actinobacteria, could control membrane fouling by pro­
ducing quorum sensing and degrading carbohydrates, respectively (Liu
et al., 2019; Maqbool et al., 2015). The lower abundance in MFC-MBR
(rGO/PPy) was possibly due to the dominant Proteobacteria and Bac­
teroidota in MFC-MBR (rGO/PPy), thereby weakened the relative
abundance of Actinobacteria. In general, a significant increase in the
abundance of Actinobacteria would alleviate membrane fouling in MFC-
MBRs. As for Firmicutes, the proportions in the three reactors were
much larger than that in the inoculated sludge (0.81 %), which indicated
that the operation condition was beneficial for the growth of Firmicutes.
Among them, the proportion of Firmicutes in MFC-MBR (PPy) and MFC-
MBR (rGO/PPy) were 4.47 %, and 5.22 %, respectively. Wrighton et al.
demonstrated the role of Firmicutes in producing electricity in MFC,
commonly known as electricity producing bacteria (Wrighton et al.,
2008). They also showed that Firmicutes were bacteria for nitrogen
metabolism, which might be related to denitrification (Knowles, 1982).
The higher abundance of Firmicutes in MFC-MBR (rGO/PPy) compared
to MFC-MBR (PPy) could be attributed to the better performance of its
conductive membrane, which enhanced electron transfer efficiency
(Zhao et al., 2019). The complex synergistic effects between these
functional microorganisms significantly enhanced the degradation of
pollutant and the power generation ability of the coupling system (Li
et al., 2019a).
The heat map at genus level is shown in Fig. 5 (B). The dominant
genera in the inoculated sludge were Marinicella, Rhodobacteraceae,
Flavobacteriaceae and Microbacteriaceae. Among the four samples, the
abundance of Rhodobacteraceae and Flavobacteriaceae in descending
order was inoculated sludge, MFC-MBR (rGO/PPy), MFC-MBR (PPy)
and CMBR (CM). Rhodobacteraceae was abundant in the ocean and
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Science of the Total Environment 907 (2024) 167827
coastal water, many of whose genera participated in the biogeochemical
cycle in the marine environment. Rhodobacteraceae was also the main
marine biofilm forming bacteria, which promoted the initial biofilm
formation (Gregory and Boyd, 2021). Flavobacteria was mostly het­
erotrophic nitrifying bacteria and aerobic denitrifying bacteria, with
high efficiency in degrading organic matter and nitrogen-containing
compounds (Lu et al., 2018). The reduced abundance in MBR meant
that the operating conditions would weaken the two bacterial genera.
However, the self-generated electric field helped maintain the stability
of these genera, leading to improved removal of organic matter. This
was also consistent with the results reported by Lu et al. (2018). Addi­
tionally, the higher abundance of Rhodobacteraceae and Flavobacter­
iaceae in MFC-MBR (rGO/PPy) could be attributed to the higher electric
field intensity, which was a result of the better conductivity of the rGO/
PPy CM.
3.4. Mechanism analysis
3.4.1. The expression of functional genes by PICRUSt2
In order to elucidate the mechanism of enhanced nitrogen removal
by self- generated electric field, functional genes and key enzymes
involved in Nitrogen metabolism were analyzed and predicted by PIC­
RUSt2 (Fig. 6). The description of relevant functional genes is shown in
Table S3. In the nitrification process, the abundance of ammonia mon­
ooxygenase (amoA), hydroxylamine dehydrogenase (hao) and mem­
brane bound nitrate reductase (narG) in descending order was MFC-
MBR (rGO/PPy), MFC-MBR (PPy) and CMBR (CM), which showed
that the electric field was conducive to the enrichment of nitrifying
bacteria. Similarly, the abundance of four key enzymes in the denitri­
fication process (cupric nitrite reductase, nirK; periplasmic nitrate
reductase, napA; nitric oxide reductase, qnorB; Nitrous oxide reductase,
nosZ)) increased with the increase of electric field intensity, which
indicated that the self-generated electric field contributed to promote
the complete denitrification process with N2 as the final product.
With the increase of electric field, there was a decrease in the
abundance of the assimilating nitrate reductase catalytic subunit
(nasAB) but an increase of Ferredoxin Nitrous acid reductase (nirA).
Dissimilatory nitrate reduction (DNR) was the NO3-N respiration of
microorganisms under hypoxic and anaerobic conditions. DNR of NO3-N
could be divided into respiratory NO3-N reduction (denitrification) and
fermentation DNR, where the fermentation products were NO2-N and
NH+ 4 -N(Nelson et al., 2016; Zhao et al., 2021). Changes in the abundance
of related genes revealed that the electric field suppressed the formation
of NO2-N while enhancing the production of NH+ 4 -N. Besides, a higher
electric field intensity led to a lower abundance of nitrite reductase
(nirB). The abundance of functional genes involved in nitrite reduction
exhibited an opposite trend to those involved in denitrification. This
R. Wang et al. Science of the Total Environment 907 (2024) 167827

Fig. 5. The abundance of microbial communities at the (A) phylum level and (B) genus level.

8
R. Wang et al.
Fig. 6. Abundance of functional genes involved in Nitrogen metabolism pathways in four samples.
could be attributed to the fact that the functional genes responsible for
the conversion of NO3-N to NO2-N were the same, but DNRA and
denitrification competed against each other in the biological denitrifi­
cation system (Nelson et al., 2016). In addition, the gene abundance of
glts and GLU were also positively correlated with the intensity of the
electric field, which meant that electric field also helped to convert NH+
4-
N into organic nitrogen. In general, compared with MFC-MBR (PPy), the
observed increase in functional gene abundance for nitrogen removal in
MFC-MBR (rGO/PPy) could be attributed to the enhanced electric field
intensity resulting from the improved conductivity of rGO/PPy CM. This
finding also agreed with the observed higher removal efficiencies of
NH+ 4 -N in MFC-MBR (rGO/PPy).
3.4.2. Mechanism analysis of pollutant removal and membrane fouling
control
As shown in Fig. 7, electrons generated by the degradation of organic
matter by anode microorganisms would be transmitted to the conduc­
tive cathode membrane through an external circuit, forming an electric
field near the membrane. At the same time, due to the negative charge of
sludge particles, there would be electrostatic repulsion between parti­
cles and conductive cathode membrane. Electrostatic repulsion could
effectively inhibit the deposition of sludge particles on the surface of the
membrane and alleviate membrane fouling rate. Since the oxygen
reduction reaction at the cathode would consume electrons, it would
affect the electrostatic repulsion force between the cathode and parti­
cles. Large current would be generated when improving the electrical
efficiency, thus improving the anti-fouling performance (Wang et al.,
2013).
In addition, this study analyzed the electricity generation capacity,
pollutant removal rate, anti-fouling performance of MFC-MBR (PPy) and
MFC-MBR (rGO/PPy), which found that the latter was superior to the
Fig. 7. Mechanism analysis of pollutant removal and membrane fouling control in MFC-MBR.
9
Science of the Total Environment 907 (2024) 167827
former. Based on previous research, stronger hydrophilicity, more
negative zeta potential and lower surface roughness of rGO/PPy CM
resulted in stronger anti-adhesion performance through XDLVO theory.
Besides, rGO/PPy CM had stronger conductivity than PPy CM (Wang
et al., 2022). High conductivity could enhance electron transfer between
microorganisms and electrode interfaces, reduce interface potential loss
and internal resistance of electron transfer in electrode materials, which
was beneficial for improving performance of MFC (Zhou et al., 2017).
The enhanced electricity generation performance elevated the electric
field strength, thereby improving the electrostatic repulsion between
negative charged pollutants and the membrane, significantly reducing
the deposition of foulants on the membrane surface, and finally allevi­
ating membrane fouling (Wang et al., 2020). Furthermore, the enhanced
electric field intensity was more conducive to stimulating microbial
activity and increasing microbial abundance, which promoted the
removal of pollutants.
4. Conclusion
MFC-MBR systems with conductive ceramic membranes (PPy CM
and rGO/PPy CM) were innovatively built to treat high salinity waste­
water. The coupling system could obtain power from wastewater (with
generated potentials of about 242 and 287 mV, respectively), achieve
higher effluent quality (with TOC removal efficiency of more than 90 %,
NH+ 4 -N removal efficiency of more than 86 %) and anti-fouling perfor­
mance than MBRs without electric field. Compared with PPy CM, rGO/
PPy CM had stronger conductivity, which led to stronger power gener­
ation capacity of MFC-MBR (rGO/PPy). The higher electric field
strength caused greater electrostatic repulsion between membrane with
foulants and more excellent anti-fouling performance. Microbial com­
munity analysis showed that MFC-MBR (rGO/PPy) had higher
R. Wang et al.
abundance of key functional bacteria compared to MFC-MBR (PPy). The
increased abundance of microorganisms and functional gene achieved
enhanced pollutant removal efficiency. This study provided strong evi­
dence that rGO/PPy ceramic membrane with excellent conductivity
could effectively improve the performance of MFC-MBR. Meanwhile,
this MFC-MBR (rGO/PPy) system had good application prospects in the
development of sustainable recycling technology for high salinity
wastewater treatment.
CRediT authorship contribution statement
Rui Wang: Data curation, Investigation, Writing – original draft.
Hong You: Supervision, Conceptualization. Binghan Xie: Funding
acquisition, Supervision. Guoyu Zhang: Supervision. Jing Zhu: Writing
– review & editing, Supervision. Weirun Li: Investigation. Xinan Dong:
Methodology, Investigation. Qiqing Qin: Methodology, Investigation.
Mengying Wang: Methodology, Investigation. Yi Ding: Supervision.
Haili Tan: Supervision. Yuhong Jia: Supervision. Zhipeng Li: Funding
acquisition, Writing – review & editing, Supervision.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgement
This study was supported by the National Natural Science Founda­
tion of China (No. 51408158, No. 52100036), the Taishan Industrial
Experts Program, the Open Project of State Key Laboratory of Urban
Water Resource and Environment, Harbin Institute of Technology (No.
QA201940, No. QA202140), and the Natural Science Foundation of
Shandong Province (No. ZR2020QE232, No. ZR2021QE119).
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2023.167827.
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