Science of the Total Environment 678 (2019) 533–542

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Science of the Total Environment

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

Enhancing the power performance of sediment microbial fuel cells by

novel strategies: Overlying water flow and hydraulic-driven
cathode rotating
Fei Guo a,b, Zongyang Shi a, Kaiming Yang a, Yan Wu a, Hong Liu b,⁎
a
School of Civil Engineering, Architecture and Environment, Xihua University, Chengdu 610039, China
b
Chongqing Institute of Green and Intelligent Technology, Chinese Academy of Sciences, Chongqing 400714, 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

• Cathodic limitations observed under

static condition in cathode fully sub-
merged SMFC.
• Overlying water flow greatly improved
performance of the fully submerged
cathode.
• Hydraulic-driven cathode rotating was
helpful to further power output im-
provement.
• ORR mainly occurred on the cathode ex-
posed to the air in the rotating cathode
SMFC.
• Identical anode performances were ob-
served in both SMFCs under different
conditions.

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

Article history: Sediment microbial fuel cells (SMFCs) are promising power sources for environmental monitoring in remote areas
Received 9 April 2019 and environment-friendly solutions to river sediment contamination. However, cathodic limitations will signifi-
Received in revised form 28 April 2019 cantly decrease power performance and limit its practical application. In this work, the control SMFC (SMFC-C)
Accepted 30 April 2019
with cathode horizontally and fully submerged below the overlying water, and the hydraulic-driven rotating cath-
Available online 1 May 2019
ode SMFC (SMFC-R) was constructed. Overlying water flow and hydraulic-driven cathode rotating as novel strate-
Editor: Huu Hao Ngo gies for SMFCs towards field applications were proposed. Results demonstrated that better power performance
under static condition was obtained in SMFC-R than in SMFC-C, that the overlying water flow could significantly in-
Keywords: crease the maximum power density (MPD) in SMFC-C over the static condition, and that the cathode rotating fur-
Sediment microbial fuel cells ther improved MPD in SMFC-R. The MPD obtained under static condition were 26.5 mW/m2 and 45.1 mW/m2 in
Hydraulic-driven rotating cathode SMFC-C and SMFC-R, which increased to 38.8 mW/m2 and 47.3 mW/m2 under water flow and cathode rotating con-
Overlying water flow dition, respectively. Analyses on cathode potential, overlying water pH and dissolved oxygen suggested severe ca-
Diminishing cathodic limitations thodic limitations in SMFC-C under static condition which could be diminished by overlying water flow.
Microbial community
However, almost no such limitations were observed in SMFC-R even under static condition, which is probably
due to the fact that the cathodic oxygen reaction in SMFC-R mainly occurred on the cathode exposed to the air rather
than on that submerged below the water. Identical anode performance was obtained in both SMFCs under different
conditions, which were not an influencing factor leading to different power performance.
© 2019 Elsevier B.V. All rights reserved.

⁎ Corresponding author.
E-mail address: liuhong@cigit.ac.cn (H. Liu).

https://doi.org/10.1016/j.scitotenv.2019.04.439
0048-9697/© 2019 Elsevier B.V. All rights reserved.
534 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542
1. Introduction
Microbial fuel cells (MFCs) are promising technology for energy re-
covery, waste treatment and nutrients recovery, which is attracting in-
creasing scientific interest (Ding et al., 2017; Do et al., 2018). As one
type of MFCs, sediment microbial fuel cells (SMFCs) are reliable power
sources in remote areas, which have already been practically used in
various ways, such as powering wireless sensors (Donovan et al.,
2008; Schrader et al., 2016), meteorological buoy (Tender et al., 2008),
communication systems (Schrader et al., 2016; Thomas et al., 2013),
and magnetometer (Arias-Thode et al., 2017). Very recently, SMFC-
based biosensor was proposed for in-situ and online monitoring of dis-
solved oxygen (DO), which has great potential as an early-warning sys-
tem for environmental risks (Song et al., 2019a). Besides, SMFCs are
cost-effective, eco-friendly and sustainable solutions to river sediment
contamination, which has been widely explored (Li and Yu, 2015). For
example, SMFCs were able to bioremediate sediments containing petro-
leum hydrocarbon (Morris and Jin, 2012), readily oxidizable organic
matter (ROOM) (Yuan et al., 2010), and polychlorinated biphenyls
and total organic carbon (Wu et al., 2019). Also, SMFCs were used to
prevent sediment bulking and black water agglomerate (Zhou et al.,
2015).
However, compared to typical MFCs, the performance of SMFCs
needs further improvement especially when they are operated for
long-term utilization. For example, the power output could maintain
at the maximum level for 24 days, and then gradually declined to a sta-
ble level around 1/6 of the peak output (Wang et al., 2012), or ~33% of
the maximum power (Ewing et al., 2017). Regarding the sediment bio-
remediation, it was reported that 29% of organic matter (after 120 days
operation), 24% of total petroleum hydrocarbon (after ~66 days opera-
tion), or 36% of ROOM (after 180 days operation) were decomposed
(Morris and Jin, 2012; Wang et al., 2012; Yuan et al., 2010). The lowered
performance is mainly ascribed to the feature of sediments, tempera-
ture, and dissolved oxygen (DO) availability and transfer rate for ca-
thodic oxygen reduction reaction (ORR) (Renslow et al., 2011; Song
and Jiang, 2018). Fortunately, oxygen in the air is ubiquitous and it is
convenient to increase oxygen availability and transfer rate to improve
SMFCs performance.
SMFCs usually consist of an anode buried in the sediment and a cath-
ode submerged below the water or floating on the overlying water sur-
face (Wang et al., 2012). When the cathode is immersed in the water,
cathodic half-cell reaction would be the main limiting factor for the
electricity generation due to the limited oxygen availability and mass
transport losses (Rismani-Yazdi et al., 2008). To obtain an appreciable
power output, external oxygen supply by aerators is one common ap-
proach, but it consumes energy and decreases the net energy recovered.
Oxygen insufficiency could also be addressed with a floating-cathode. It
was demonstrated that the floating-biocathode SMFC even could gener-
ate a higher power density than the control SMFC, because the floating-
cathode increased oxygen availability (Wang et al., 2012).
Interestingly, a rotating cathode was proposed in a river sediment
microbial fuel cell constructed in the laboratory, leading to a higher
maximum power density (MPD) of 49 mW/m2 compared to the non-
rotating cathode system (29 mW/m2) (He et al., 2007). In another rotat-
ing cathode MFC, maximum power output was increased by 44.4% over
the control system (Suor et al., 2014). The increased power performance
could be ascribed to the enhanced electron transfer rate, OH– transport
and O2 diffusion under the rotating conditions (Chen et al., 2018). Be-
sides, rotating cathode was helpful to achieving simultaneous carbon
and nitrogen removal (Sayess et al., 2013; Zhang et al., 2013). However,
the cathode rotating driven by motors would consume energy and in-
crease the capital costs as well, although it is a potential strategy for
MFC performance improvements. For example, a power consumption
around 4 W/m3 was suggested when the cathode was rotating at
8 rpm, which substantially decreased the net power density harvested
by MFCs (Suor et al., 2014). So, as suggested by Chen et al. (2018), it
would be more economically practical to drive an air-cathode rotating
by hydraulic energy or water movement, and the field conditions of riv-
ers could be well suited to such strategies towards practical
applications.
Water flow velocity in rivers, hydrostatic heads of waterfalls and the
ocean waves are potential energy sources that have been practically
converted to electricity for household applications and remote environ-
mental monitoring (Dewan et al., 2014). Compared to the conversion of
hydraulic energy to electricity, the direct use of the energy, for example,
to drive a cathode rotating, would be more advantageous, because it
saves the capital costs on energy convertor. Also, the cathode rotating
driven by hydraulic energy saves running cost compared to by motors.
What's more, SMFCs would be constructed in rivers in remote areas
for practical applications in future where the power grids for motors
used to drive cathode rotating are most likely uninstalled there, other-
wise there are no needs to construct SMFCs as power sources for envi-
ronmental monitoring. Hence, the alternative driving force for cathode
rotating in SMFCs should be explored, and it will be more practical to
convert the hydraulic energy to mechanical energy, driving the cathode
of SMFCs rotating.
Water flow in rivers is everlasting, and it is not difficult to accept that
water flow from upstream to downstream and water movement caused
by wind blowing could accelerate atmospheric reoxygenation of the
overlying water, increasing oxygen availability and transfer rate at the
cathode of the SMFCs deployed in rivers. However, at this stage SMFCs
were usually constructed and operated in laboratories with overlying
water under static condition, neglecting the oxygen availability and
transfer resulted from the water flow under field conditions. So, the
overlying water flow should be taken into account and used as an
inartificial strategy for power performance improvement in SMFCs.
In summary, the overlying water flow and hydraulic energy in rivers
where the SMFCs usually deployed are extremely common and could be
easily captured. In this work, the overlying water flow would be mim-
icked, and a novel rotating cathode driven by hydraulic energy was con-
structed and installed in SMFCs to enhance power performances. The
goal of this work was to demonstrate the feasibility of improving
power performance of SMFCs by the overlying water flow and cathode
rotating driven by hydraulic-energy. Such strategies will push forward
the field applications of SMFCs. The SMFCs performance under static
and overlying water flow or cathode rotating conditions would be com-
pared in terms of voltage output, cathode potential, polarization curves
and power density. Dissolved oxygen (DO) in the overlying water, an
important influencing factor, would also be analyzed. Finally, the bacte-
rial communities of the anodic biofilms in SMFCs would be identified.
2. Materials and methods
2.1. Construction of SMFCs
In this work, the control SMFC (SMFC-C) with a cathode horizon-
tally and fully submerged below the overlying water and the
cathode-rotating SMFC (SMFC-R) driven by hydraulic energy were
constructed. The SMFCs were deployed in cylindrical containers
with diameter and depth of 22 cm and 26 cm, respectively. The
anodes of both SMFCs were made of carbon felt (L × W × H: 10 cm
× 10 cm × 0.5 cm). The cathode of the SMFC-C was a piece of carbon
cloth (L × W: 8 cm × 2 cm), two sides exposed to the overlying water,
resulting in a working surface area of 32 cm2. The hydraulic-driven
rotating cathode used in SMFC-R was mainly composed of two
water wheels, one supporting cylinder and a piece of carbon cloth
coated with platinum (Fig. 1). Platinum was coated on the cathodes
with a loading rate of 0.5 mg Pt/cm2 . The cathode of the SMFC-R
was also made of carbon cloth (L × W: 16 cm × 2 cm) which was
wrapped around a supporting cylinder with diameter of 5 cm
(Fig. 1). Since one side of the rotating cathode was exposed to the
overlying water or the air, available for cathode reduction reaction,
 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542
Fig. 1. Schematic diagram of the hydraulic-driven rotating cathode used in SMFC-R.
the cathodes of both SMFC-C and SMFC-R had same working surface
area (32 cm2). The cathode would be rotated driven by the falling
water on the water wheels, namely hydraulic-driven rotating cath-
ode in this work. A total falling water flow rate of ~125 L/h on the
water wheels was adopted, leading to a rotation speed ranging
from 16 rpm to 20 rpm.
The bottom of the SMFCs was filled with sediments collected from a
pond at the Xihua University. The depth of the sediment layers were
12 cm and the anodes were placed 6 cm below the sediment/water in-
terfaces. The sediments were covered with water collected from the
same pond, working as catholyte, and the height of the overlying
water was 8 cm. To maximize the oxygen availability, the cathode of
SMFC-C was horizontally placed 5 mm below the water/air interface,
fully submerged below the overlying water. The cylindrical cathode of
MFC-R was 50% submerged in the water and the other 50% was exposed
to the air. All experiments were conducted using identical SMFCs in
duplicate.
2.2. Start-up and operation
The SMFCs were connected to a 1000 Ω external resistance, and
started up at room temperature (~17 °C). From day 12 onwards, the
SMFCs were put in an external container to control the overlying
water temperature in the SMFCs at 21 ± 1 °C by means of water bath
heating, and the temperature of water in the external container was at
25 ± 1 °C. The water lost through evaporation was supplemented
everyday.
The whole experiment was divided into 5 stages as introduced in
Table 1. Overlying water flow was simulated using the aquarium
water pumps, exchanging water between cathode compartments and
the external container. Water flow and cathode rotating in both
SMFC-C and SMFC-R was intermittently turned on and turned off at
the same time. In one cycle, the water flow and cathode rotating was
first conducted for 1 h, and then both systems were switched to static
conditions for the next 3 h, forming a whole cycle with 4 h in total. Cath-
ode rotating in SMFC-R was driven by the falling water on the water
wheels, which would also result in water flow at the same time.
Table 1
Condition switches in SMFC-C and SMFC-R.
SMFC Conditions Stage 1 Stage 2 Stage 3 Stage 4
SMFC-C Water flow NO YES NO NO
SMFC-R Water flow NO YES NO NO
Cathode rotating NO NO NO NO
535
Therefore, it should be noted that no additional water flow was carried
out in SMFC-R in stage 5. Identical flow rates were adopted in both
SMFCs.
2.3. Electrochemical and chemical analysis
Cell voltage (V), across a fixed external resistance of 1000 Ω was col-
lected every 2 min by a data acquisition system (PISO-813 U, Hongge
Taiwan) and recorded in a personal computer. The current (I) was cal-
culated according to Ohm's law, I=V/Rext, where Rext is the fixed external
resistance: Rext = 1000 Ω. Power was calculated by multiplying voltage
with current, P=V × I. Power densities (PA) were calculated by dividing
the power by working surface area of the cathode, PA = P/Acat, where
Acat is 32 cm2. The polarization curves were obtained by varying the ex-
ternal resistances, decreased from 10,000 Ω to 400 Ω after the systems
reached stable conditions. Meanwhile, the cathode potentials (Pcat)
were recorded with the assistance of Ag/AgCl reference electrodes
(RE-1C, Jiangfen Tech Co. Ltd., Jiangsu, China; +197 mV, vs standard hy-
drogen electrode, SHE). The anode potentials (Pan) were calculated
using the following equation: Pan = Pcat -V. The slopes of ohmic region
in the polarization curves were taken as the internal resistances (Rint).
In stage 4 and stage 5, cathode potential was recorded every 2 min
using digital multimeters. pH and DO was detected using benchtop me-
ters (Sanxin MP551, China).
2.4. DNA extraction and PCR amplification
At the end of the experiments, anodic biofilms samples were col-
lected for DNA extraction. For both SMFCs, 9 cm2 anode enriched with
electricity-generating bacteria was cut from the enriched anode for
DNA extraction. DNA of the original pond sediment community was
also extracted to make comparisons.
Microbial DNA was extracted using the E.Z.N.A.® soil DNA Kit
(Omega Bio-tek, Norcross, GA, USA) according to the manufacturer's
protocols. The V3-V4 region of bacteria 16S ribosomal RNA gene were
amplified by PCR with the primers set 338F (5′-barcode-CCTACGGGA
GGCAGCAG-3′) and 806R (5’-GGACTACHVGGGTWTCTAAT-3′). PCR
was carried out in an ABI GeneAmp®9700 (Applied Biosystems, USA)
with the following steps: initial denaturation at 95 °C for 3 min,
followed by 27 cycles of denaturing at 95 °C for 30 s, annealing at 55
°C for 30 s, extension at 72 °C for 45 s, and a final extension at 72 °C
for 10 min. PCR reactions were performed in triplicate 20 μL mixture
containing 4 μL of 5× FastPfu Buffer, 2 μL of 2.5 mM dNTPs, 0.8 μL of 5
μM Forward Primer, 0.8 μL of 5 μM Reverse Primer, 0.4 μL FastPfu Poly-
merase and 10 ng Template DNA.
2.5. Bacterial communities
Amplicons were extracted from 2% agarose gels, purified using the
AxyPrep DNA Gel Extraction Kit (Axygen Biosciences, Union City, CA,
USA) according to the manufacturer's instructions, and quantified
using QuantiFluor™-ST (Promega, USA). Purified amplicons were
pooled in equimolar and paired-end sequenced on an Illumina MiSeq
platform according to the standard protocols. The raw reads were de-
posited into the NCBI Sequence Read Archive (SRA) database. Raw
fastq files were demultiplexed and quality-filtered using QIIME (version
1.9.1).
The phylotypes in communities were clustered into operational tax-
onomic units (OTUs) at 97% similarity (equivalent to 0.03 sequence dis-
tance) using UPARSE. The taxonomy of each 16S rRNA gene sequence
Stage 5
was analyzed using RDP Classifier with 70% confidence threshold. To an-
YES alyze alpha-diversity and richness, Shannon, Simpson, Chao and Ace
YES were calculated. Dominant bacterial communities were analyzed at
YES
level of phylum, class and genus, respectively.
536 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542

3. Results and discussion
3.1. Voltage output and power density
3.1.1. Voltage output
As shown in Fig. 2, voltages in SMFC-C and SMFC-R quickly increased
to 100 mV and 120 mV within the first 12 h, respectively. Afterwards, it
experienced ups and downs in SMFC-C, while gradually increased and
arrived at a stable level in SMFC-R. From day 12 onwards, sharp in-
creases in voltages were observed when the overlying water tempera-
tures were maintained at 21 ± 1 °C by means of water bath heating.
The following investigations were divided into five stages (Table 1).
In stage 1, maximum voltage was higher in SMFC-R than in SMFC-C,
and voltages in SMFCs underwent totally different changing patterns.
Specifically, SMFC-R generated a maximum voltage up to 380 mV with
slight fluctuations. However, voltage in SMFC-C periodically changed
from 150 mV to 340 mV, which is worth of further observations
(Fig. 2A). In stage 2, the overlying water flow in both SMFC-C and
SMFC-R was mimicked by means of water exchanging between the
cathode chambers and the external container. Compared to stage 1, ob-
viously narrowed difference in voltages between SMFC-C and SMFC-R
was demonstrated (Fig. 2). In MFC-C, a waving changing pattern was
observed as the overlying water was intermittently flowing (Fig. 2B).
In each cycle, voltage quickly increased over the first 1 h, and then grad-
ually decreased during the following 3 h till the SMFCs were switched to
water flow conditions again. However, the overlying water flow did not
significantly change the voltage output in SMFC-R (Fig. 2B).
0.40 stage 1
A
0.35
0.30 Temperature
o
controlled at 25 1 C
Voltage (V)
In stage 3, SMFCs were maintained under static conditions, and the
huge difference in power performance was observed again as that in
stage 1. Results demonstrated that SMFC-R generated a more stable
and higher voltage, and that voltage in SMFC-C fluctuated with a
much narrower range under water flow condition (stage 2) than
under static conditions (stage 1, stage 3). Since both SMFCs had same
anodes and operating environments, the higher voltage in SMFC-R
should be attributed to the different cathode configuration. It has been
demonstrated that SMFC with a comb-type cathode that is partially ex-
posed to the air had better power performance (Wang et al., 2017). In
another SMFC equipped with a wicking air cathode, 50% of the cathode
suspended above the column and the rest 50% submerged below the
water, voltage output was much more stable and higher than that in a
SMFC with a fully submerged cathode (Morris and Jin, 2012). In this
work, a cylindrical cathode was used in SMFC-R, 50% of the cathode ex-
posed to the air and the other 50% submerged below the water. There-
fore, the findings in this work were in consistency with those in the
literature (Morris and Jin, 2012; Wang et al., 2017).
Since the anodes were placed inside the sediments where the envi-
ronments could hardly be influenced by the overlying water flow, the
cathode potentials were collected, which would cast light on the voltage
profiles. Voltage and cathode potential under static condition were re-
corded at the same time in stage 4. As shown in Fig. 3, both voltage
and potential in SMFC-C fluctuated within huge ranges as presented
above (Fig. 2A). Similarly, more stable and higher voltage and cathode
potential were observed in SMFC-R. It should be noted that the breaks,
missing data in Fig. 3 were resulted from the power outage.
Voltage and cathode potential under water flow and cathode rotat-
ing conditions were collected in stage 5. Similar as in stage 2, voltages
stage 2 stage 3 accordingly changed with the water flow and the cathode rotating in
SMFC-C and SMFC-R, respectively (Fig. 4A). Results indicated that
higher voltage was obtained in SMFC-R than in SMFC-C, that water
flow and cathode rotating increased voltage and cathode potential
over the first 1 h in each cycle, and that water flow enabled MFC-C to

0.25 produce a more stable voltage. The improved cathode performance

0.25
0.20 under water flow or cathode rotating conditions was in consistency
with the findings in the literature (Chen et al., 2018). On one hand, cath-
0.15 ode potential was temporarily higher in SMFC-C than in SMFC-R, which
0.15
0.10 was different from that observed in stage 4 (Figs. 3, 4B). But, when the
SMFC-R duration of static condition was extended to 7 h in the last cycle, cath-
0.05 SMFC-C ode potential kept decreasing in SMFC-C, while maintained constant
in SMFC-R, and significant difference was observed again (Fig. 4B).
0.00
The findings here suggested that it is important to adopt proper
0 4 8 12 16 20 24 28 32 36
Time (day)
SMFC-R SMFC-C SMFC-R/V SMFC-R/P
0.37
B SMFC-C/V SMFC-C/P
0.36 0.40 0.40
0.36
Cathode potential vs Ag/AgCl (V)

0.35 0.35
0.32
0.34 0.30
0.28
Voltage (V)

0.33 0.25
0.24
Voltage (V)

0.32 0.20 0.20

0.31 0.16 0.15
0.30 0.12
0.10
0.29 0.08
0.04 0.05
0.28
0.00 0.00
0.27
-0.04 power outage
-0.05
0.26 -0.08
0 2 4 6 8 10 12 14 16 18 20 22 24 -0.10
Time (h) 0 1 2 3 4 5
Time (day)
Fig. 2. Voltages in SMFCs during the start-up period, stage 1, stage 2, and stage 3 (A), and
during the last 6 cycles of stage 2 (B). In each cycle, overlying water flow was conducted Fig. 3. Voltages and cathode potentials in SMFCs under static condition, observed in stage
over the first 1 h and followed by static condition over the next 3 h. 4.
 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542
SMFC-R SMFC-C
0.48
0.44
0.40
0.36
Voltage (V)
0.32
0.28
0.24
0.20
0.16
0.12
Static
0.08
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28
Time (h)
0.32 SMFC-R SMFC-C
Potential vs Ag/AgCl (V)
0.28
0.24
0.20
0.16
0.12
0.08
Static
0.04
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28
Time (h)
Fig. 4. Voltages (A) and cathode potentials (B) under intermittent water flow (SMFC-C)
and cathode rotating (SMFC-R) conditions, observed in stage 5. In each cycle, overlying
water flow or cathode rotating was conducted over the first 1 h and followed by static
condition over the next 3 h. Both SMFCs were operated under static condition for 7 h in
the last cycle as indicated with blue lines.
operating strategies to obtain higher power performance. The cathode
potential profiles also suggested that the higher mass transport losses
under static condition in the cathode unit of SMFC-C were resulted
from the insufficient convection and diffusion in catholyte, the overly-
ing water (Rismani-Yazdi et al., 2008). Therefore, the overlying water
flow proposed in this work is an efficient strategy to enhance mass
transport and cathode reaction performance, especially for SMFCs
with fully submerged cathode. It is a practical and cost-efficient strategy
towards field applications when the SMFCs would be deployed in rivers.
3.1.2. Power densities and polarization curves
As shown in Fig. 5, power density, polarization curve and electrode
potential significantly changed in SMFC-C under different conditions,
while slightly increased in SMFC-R when the cathode was rotating. Spe-
cifically, the MPD increased from 26.5 mW/m2 to 38.8 mW/m2 (in-
creased by 46.4%) when the overlying water was flowing in SMFC-C
(Fig. 5A). However, the MPD in SMFC-R slightly increased from
45.1 mW/m2 to 47.3 mW/m2 when the condition was switched from
the static to cathode rotating (Fig. 5C). Under static condition, the
MPD in SMFC-R was 70.2% more than that in SMFC-C (45.1 mW/m2 vs
26.5 mW/m2). The internal resistances were estimated around 2086 Ω
(static), 883 Ω (water flow) and 1090 Ω (static), 905 Ω (rotating) in
SMFC-C and SMFC-R, respectively. Internal resistance reduced by
57.7% (SMFC-C) and 17.0% (SMFC-R) when the overlying water was
flowing and the cathode rotating, respectively. Internal resistance in
SMFC-C was 1.91 times as high as that in SMFC-R under static condition
537
and the difference was significantly narrowed when the novel strategies
A were carried out.
In SMFC-R, compared to the static condition, slight increase (4.9%) in
MPD was observed under cathode rotating condition, which was lower
than that reported in the literature. For example, it was reported that
MPD increased by 44.4% (Suor et al., 2014), and by 69% (He et al.,
2007) in the rotating cathode MFCs over the control system. The in-
creased MPD and voltage was attributed to the improved cathode po-
tentials under rotating condition, which was around 2 times as high as
that under the control condition, probably suggesting that the cathodic
overpotential under static condition deteriorated the overall power per-
formance and cathode rotating improved cathode performance signifi-
cantly (He et al., 2007). The cathode performance and MPD improved
more significantly in the literature were probably resulted from the
cathode materials and structures used in SMFCs, because the rotating
cathodes with thicker structures (3-dimensional) were made of carbon
felt (Suor et al., 2014), and reticulated vitreous carbon (He et al., 2007).
Compared to the static condition where the cathodic ORR mainly takes
B
place on the surface of the cathode, the cathode rotating could acceler-
ate mass transfer and facilitate oxygen transferring from exterior to in-
terior of the thicker cathodes that will activate the carbon active sites
inside the electrodes for ORR and finally enhance power performance
of SMFCs (Merino-Jimenez et al., 2016). Therefore, the high increase in
power densities reported in the literatures might be in part due to the
increased working cathode sizes under rotating conditions. In the pres-
ent work, since a piece of carbon cloth with a much thinner structure
was wrapped around a cylinder, the majority of the active sites for
ORR are ready and available even under static condition as demon-
strated by the cathode potentials (Fig. 5D). Thus, the cathode rotating
in SMFC-R did not increase MPD significantly. In this work, cathode po-
tential slightly increased at current densities higher than 76.4 mA/m2
(Fig. 5D), which demonstrated that the cathodic limitations were negli-
gible in SMFC-R even under static condition. Namely, the cathodic ORR
was not limited by oxygen availability or oxygen transfer rate, which
suggested that the cathodic ORR mainly occurred on the cathode ex-
posed to air where there was considerable oxygen available for ORR.
Fig. 5D also demonstrates no significant variations in anode potentials
under both conditions and anodic overpotential at current density
higher than 120 mA/m2, which was likely resulted from the limited
mass transport in the anode unit. Moreover, anode potentials in both
SMFCs under all conditions were in similar level (Fig. 5B, D), indicating
that the anode performance did not vary with the strategies applied to
the cathode units and were probably not responsible for the difference
in power performance between SMFC-C and SMFC-R.
In SMFC-C, Fig. 5A and C shows an increased MPD and improved
cathode performance under water flow condition compared to static
condition. An increase of 46.4% in MPD was slight higher than that ob-
served by Suor et al. (2014), and lower than that reported by He et al.
(2007). Since the cathode was horizontally and fully submerged
below the water, severe cathodic overpotential or mass transport losses
under static condition was demonstrated because of low DO and deteri-
orated oxygen transfer rate. An improved cathode performance and
MPD was obtained as expected under water flow condition. The differ-
ence in cathode potential profiles under different conditions was in
agreement with previous finding in the literature (He et al., 2007). In
addition, no significant difference in anode potentials was observed.
Therefore, the overlying water flow is an efficient and easy-to-operate
strategy to diminish cathodic limitations and improve power perfor-
mance of SMFCs. On the other hand, MPD in SMFC-C under water flow
condition is still lower than that in SMFC-R, indicating that rotating
cathode SMFCs could further increase power performance.
3.2. pH, temperature and DO profiles
To explore the main factors changing the voltage and cathode poten-
tial under different conditions, the overlying water pH, temperature and
538 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542

50 50
600 A SMFC-C/PD-Water flow 45
600 C 45
SMFC-C/PD-Static
500 40 40
500
35

Power density (mW/m )

35

Power density (mW/m )

2
2
Voltage (V)

Voltage (V)
400 400 30
30

25 25
300 300 SMFC-R/V-Static
20 SMFC-R/V-Rotated 20
200 15 200 15
SMFC-C/V-Water flow
SMFC-C/V-Static 10 10
100 100
SMFC-R/PD-Static 5
5
SMFC-R/PD-Rotated
0 0 0 0
0 20 40 60 80 100 120 140 160 180 0 20 40 60 80 100 120 140 160
2 2
Current density (mA/m ) Current density (mA/m )

300
B 300
D
200 200
SMFC-C/CP-Water flow
Potential vs Ag/AgCl (V)

Potential vs Ag/AgCl (V)

SMFC-C/CP-Static
100 100 SMFC-R/CP-Rotated
SMFC-R/CP-Static
0 0

-100 SMFC-R/AP-Rotated
-100
SMFC-R/AP-Static

-200 -200
SMFC-C/AP-Water flow
-300 -300
SMFC-C/AP-Static

-400 -400
0 20 40 60 80 100 120 140 160 180 0 20 40 60 80 100 120 140 160
2 2
Current density (mA/m ) Current density (mA/m )

Fig. 5. Power density and polarization curves (A,C), and electrode potentials (B,D) as a function of current density observed in SMFC-C (A,B) and SMFC-R (C,D) under static and water flow
condition in SMFC-C (or cathode rotating in SMFC-R). V: Voltage; PD: Power density; AP: Anode potential; CP: Cathode potential.

DO was continuously detected for 24 h. As widely accepted, pH shifts anode to the cathode, and that proton and electron generated in the
could be observed in MFCs with membranes, and anolyte and catholyte anode chambers equaled to that consumed at the cathodes. However,
will be getting more acidic and more alkaline, respectively (Fornero as shown in Fig. 6, higher catholyte pH was observed in SMFC-C under
et al., 2010). Theoretically, the overlying water pH in both SMFCs in static condition, suggesting the alkalinity accumulation due to the lack
this work should be identical due to the fact that no membranes were of buffer system. The difference could be explained as follows. In
used to separate two chambers, facilitating proton transfer from the SMFC-R, the 50% cathode exposed to the air maintained wet that was

SMFC-C/Water flow SMFC-R/Rotated

SMFC-C/Static SMFC-R/Static
7.8 7.8
A B
7.6 7.6

7.4 7.4

7.2 7.2
pH
pH

7.0 7.0

6.8 6.8

6.6 6.6

6.4 6.4

6.2 6.2
0 2 4 6 8 10 12 14 16 18 20 22 24 0 2 4 6 8 10 12 14 16 18 20 22 24
Time (h) Time (h)

Fig. 6. Catholyte pH in SMFC-C (A), and SMFC-R (B) under static and water flow (or cathode rotating) conditions, detected in stage 4 and stage 5, respectively (presented as mean ±
standard deviation, n = 2). In each cycle, overlying water flow or cathode rotating was conducted over the first 1 h and followed by static condition over the next 3 h.
 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542
a preferable place for cathodic ORR, probably enabling CO2 from the air
to participate in the cathode reactions and thus preventing catholyte
alkalization. It has been suggested that CO2 reacts with hydroxide ions
produced by the cathodic ORR and forms carbonate or bicarbonate, fi-
nally building a CO2/carbonate or (and) CO2/bicarbonate buffering sys-
tem (Fornero et al., 2010; Torres et al., 2008). In SMFC-C, since the
cathode was fully submerged below the water surface, no such buffer-
ing systems could be built up and thus resulted in an increasing in
water pH.
When water flow and cathode rotating was intermittently con-
ducted, pH rapidly increased over the first 1 h in each cycle and then de-
creased, finally led to identical overall pH levels in SMFC-C and SMFC-R
(Fig. 6). Generally, pH decreased and higher voltage was produced in
SMFC-C, it could be due to the fact that catholyte flow or recirculation
was able to buffer pH condition (Wang et al., 2018). On the other
hand, as has been demonstrated that catholyte pH plays an important
role in cathode potential and MFC power performance (Erable et al.,
2009), different voltage outputs in SMFCs under static condition should
be partially ascribed to difference in pH.
Besides, similar changing trends in the overlying water temperature
and DO were observed (Fig. 7). They first quickly increased during the
first 1 h when the overlying water was flowing and cathode rotating,
and then gradually decreased over the next 3 h under static condition.
Concerning the difference in water temperature, SMFCs were placed
in an external container and temperature was controlled by means of
water bath heating. Temperature of catholyte was 21 ± 1 °C under static
condition, lower than that in the external container (25 ± 1 °C). Accord-
ingly, catholyte temperature increased when the overlying water in the
cathodes was exchanged with that in the external container (Fig. 7A).
However, it has been demonstrated that temperature ranging from 20
°C to 32 °C would hardly influence the power generation in MFCs with
platinum catalyzed air-cathode (Liu et al., 2005). Therefore, an increase
of ~4 °C in water temperature in this work might not be a primary con-
tributor to the increased performance of SMFCs.
As shown in Fig. 7B, DO in the overlying water in both SMFCs was
relative constant and comparable under static condition. Sudden in-
creases and much higher DO were observed when the systems were
switched to water flow and cathode rotating conditions. One hour
later, DO was started to gradually decrease over the next 3 h. Comparing
the DO at the beginning of one cycle to that at the end of the previous
cycle, water flow and cathode rotating could increase DO by 179.2 ±
46.7% and 262.5 ± 40.2%, from 2.56 ± 0.28 mg/L to 7.0 ± 0.56 mg/L
SMFC-C/Static
SMFC-C/Water flow
26
25
T e m p e ra tu re ( C )
24
o
23
22
21
20
0 2 4 6 8 10 12 14 16 18 20 22 24
Time (h)
Fig. 7. Temperature (A), and DO (B) of catholyte under static and water flow (or cathode rotating) conditions, detected in stage 4 and stage 5, respectively (presented as mean ± standard
deviation, n = 2). In each cycle, overlying water flow or cathode rotating was conducted over the first 1 h and followed by static condition over the next 3 h.
539
and from 1.93 ± 0.36 mg/L to 6.86 ± 0.54 mg/L in SMFC-C and SMFC-
R, respectively.
As has been suggested previously (Chen et al., 2018; He et al., 2007;
Rismani-Yazdi et al., 2008), the overlying water flow significantly in-
creased oxygen concentration and mass transfer rate, which was the
primary contributor to the improved power output in SMFC-C. In prac-
tice, it is easy to use water flow in river SMFCs to produce stable and
higher power. In SMFC-R, multiple aspects should be taken into account
to analyze how water flow or cathode rotating affects power perfor-
mance. First, oxygen concentration is much higher in air than in
water. Thus, massive oxygen is available for ORR on the cathode ex-
posed to the air where the cathodic reduction is preferably occurring
(Morris and Jin, 2012; Wang et al., 2017). That is why no cathodic limi-
tations were observed and better power performance could be obtained
even under static condition in SMFC-R. Second, DO in catholyte in-
creased when the cathode was rotating, but still much lower than that
in air. So, the temporarily increased voltage output might be due to
the enhanced mass transport rate rather than the increase in oxygen
availability in the overlying water.
To sum up, in SMFC-R, the stable and higher cathode performance
and power generation under static condition is mainly due to the ex-
posed cathode with plenty oxygen availability from the air. The pH buff-
ering system built up on the exposed cathode is also responsible for the
better power performance. The temporary increase in voltage was as-
cribed to the enhanced oxygen transfer rate when the cathode was ro-
tating. In SMFC-C, the overlying water flow could significantly increase
oxygen concentration and transfer rate as well, which jointly stabilized
and increased power output. The decreased overlying water pH is also
beneficial to improve cathode performance in SMFC-C. Generally, the
overlying water flow and cathode rotating are practically feasible strat-
egies for power improvement in SMFCs towards field applications. Also,
it was demonstrated that the hydraulic energy could be utilized as alter-
native driving force for rotating cathode SMFCs, which could further im-
prove power performance.
3.3. Microbial community analysis
The microbial communities associated with the original sediment
and the SMFC anodes were analyzed to gain insights into whether the
anodic biofilms are different and influence the power generation in
SMFCs. Fig. 8A shows the saturated rarefaction curves, suggesting that
almost all species were discovered in the bacterial analysis. Regarding
SMFC-R/Static SMFC-C/Static SMFC-R/Static
SMFC-R/Rotated SMFC-C/Water flow SMFC-R/Rotated
A 8 B
7
6
D O (m g /L )
5
4
3
2
1
0
0 2 4 6 8 10 12 14 16 18 20 22 24
Time (h)
540 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542

1200 Phyla Nitrospirae and Nitrospinae as the nitrite-oxidizing bacteria

A (Pachiadaki et al., 2017), however were obviously enriched in the an-
1000 odic biofilms of SMFCs (Fig. 8B) and their effects on the electricity gen-
eration remaining to be discovered. In addition, phyla Bacteroidetes,
800 Actinobacteria and Firmicutes were also identified here which would
Number of OTUs

also be able to oxidize organics in the sediment, releasing electron for

600 Orginal sediment power production.
Anodic biofilm in SMFC-C The deeper analyses of the 16S rRNA gene sequences at the genus
400 Anodic biofilm in SMFC-R
level revealed that the electricity-generating biofilms were dominated
by Desulfobulbus with relative abundance of 13.3% in SMFC-C and 8.1%
200 in SMFC-R, respectively. Also, two uncultured genera belonging to
phyla Cyanobacteria and Chloroflexi were observed, accounting for
0 5.4% and 10.8%, 4.3% and 8.8% in SMFC-C and SMFC-R, respectively,
which should also contribute to electricity generation. However, as
0 5000 10000 15000 20000 25000 30000
one of the most common electricity-generating bacterium, the genus
Number of reads sampled
Geobacter hardly enriched with low relative abundance of 1.4% and
50
B 1.3% in SMFC-C and SMFC-R, respectively, which was in agreement
45 with the findings in ordinary SMFCs previously reported (Ewing et al.,
Orginal sediment
40 Anodic biofilm in MFC-C 2017; Lu et al., 2015). On the other hand, better enrichments of
Relative abundance (%)

Anodic biofilm in MFC-R Geobacter species could be obtained in SMFCs with 3-D Microemulsion
35
doped anodes (Ewing et al., 2017), or in plant-based SMFCs (Cabezas
30 et al., 2015; Lu et al., 2015), providing strategies to improve Geobacter
25 enriching in SMFCs. In general, comparable anodic biofilm structures
20 were identified in both SMFCs, which were the fundamental reason
for the identical anode performance obtained in SMFCs (Fig. 5B, D).
15
Thus, identical anode performance was observed in SMFC-C and
10 SMFC-R, which probably would not an influencing factor for the differ-
5 ent power performance between SMFC-C and SMFC-R.
0
ia xi ia ae inae detes teria cutes thers 3.4. Practical implications
cter ofle cter spir p i c i
oteoba Chlor anoba Nitro Nitros actero tinoba Firm O
Pr Cy B Ac
Strategies such as the overlying water flow and hydraulic-driven ro-
tating cathode were proposed to obtain more stable and higher voltage
Fig. 8. Rarefaction curves of OTUs (A), and sequence distribution at the phylum level in generation that could be used to power environmental sensors in re-
clone libraries of 16S rRNA genes amplified from the microbial communities associated
mote areas (Arias-Thode et al., 2017; Dewan et al., 2014; Schrader
with the original sediment and the anodic biofilms in SMFC (B).
et al., 2016; Tender et al., 2008; Thomas et al., 2013). Rotating cathode
in this work was driven by hydraulic energy, which could be easily har-
vested and accordingly saves the running cost, for example, the energy
the bacterial diversity, multiple indicators demonstrated comparable consumption by a motor used to drive a cathode rotating. The rotating
diversities of the anodic biofilm communities in SMFC-C and SMFC-R, cathode configuration could combine well with the local environments,
both of which was slightly improved compared to that in the original and directly use the hydraulic energy on site for power performance im-
sediment (Table 2). provement in SMFCs, pushing SMFCs technology forward field applica-
As shown in Fig. 8B, the dominant bacteria at the phylum level were tions. Power production in SMFCs was originally converted from the
Proteobacteria in original sediment (53.4%), SMFC-C (32.8%) and SMFC- degradation of the organic matters in the sediment layer. More stable
R (29.2%). As widely reported elsewhere (Cabezas et al., 2015; Ewing and higher voltage generation means that organics in the contaminated
et al., 2017; Lu et al., 2015), Proteobacteria were suggested as the main sediment could be more efficiently biodegraded (Suor et al., 2014).
exoelectrogens in this work, but probably not a factor for the difference Therefore, the overlying water flow and cathode rotating are also prom-
in power performance between SMFC-C and SMFC-R because of the ising strategies for efficient sediment bioremediation.
almost same abundance level. Regarding phyla Chloroflexi and Excess nitrogen in water body is considered as one of the primary
Cyanobacteria, higher relative abundances were observed in SMFC-R causes of eutrophiciation, and extensive researches have been done to
than in SMFC-C, 14.7% vs 10.8% and 11.2% vs 6.1%, respectively, which obtain a cost-effective and efficient nitrogen removal (McCarty, 2018;
might be resulted from the different cathode configurations and thus Sepehri and Sarrafzadeh, 2018; Song et al., 2019b). Interestingly, it
in part changed the power performance. Interestingly, Cyanobacteria was demonstrated that it is feasible to using a rotating cathode in
were also identified in the present SMFCs and it has been demonstrated MFCs or bioelectrochemical contactor to removal organic matters, nitro-
that Cyanobacteria were capable of generating electricity in SMFC (Zhao gen and suspended solids (Sayess et al., 2013; Suor et al., 2014; Zhang
et al., 2012), and in photosynthetic MFC as well (Kaushik et al., 2017). et al., 2013). Nitrogen could be removed through simultaneous nitrifica-
tion and denitrification processes with a rotating cathode that is inter-
mittently exposed to the anoxic and aerobic condition. In constructed
wetland MFCs with a similar reactor configuration to SMFCs, DO in the
Table 2
cathode zone was significant for organics and nitrogen removal
Alpha-diversity of microbial communities in the original sediment and the anodic biofilm
(AB) in SMFC-C and SMFC-R. (Wang et al., 2019). It should be noted that the abiotic cathode with
platinum as catalyst was used in SMFC-R. However, in future the
Samples OTU Shannon Simpson Ace Chao Coverage
SMFC-R could be equipped with a hydraulic-driven rotating biocathode
Orginal sediment 917 5.38 0.017 968 976 0.996 using bacteria instead of platinum as catalyst, and the increased DO con-
AB in SMFC-C 967 5.31 0.016 1023 1031 0.996 centration in the cathode chambers would be helpful to organics and ni-
AB in SMFC-R 1080 5.54 0.014 1094 1101 0.999
trogen removal through biological pathways. Besides, compared to the
 F. Guo et al. / Science of the Total Environment 678 (2019) 533–542
abiotic cathodes using noble metal catalysts, the biocathodes will make
SMFCs more sustainable and eco-friendly (Wang et al., 2012). Further-
more, as mentioned above, phyla Nitrospirae and Nitrospinae as the
nitrite-oxidizing bacteria were identified in the anodic biofilms,
which would participate in nitrogen cycling and nutrients removal as
well in the sediment of SMFCs, finally contributing to the alleviation of
water eutrophication. Therefore, it is also a potential solution to eutro-
phic water body resulted from the exceeded nitrogen concentration.
Last, as one compartment of the rotating cathode in SMFCs, water
wheels could work as a landscape, improving the ornamental effect of
SMFCs.
The overlying water flow is everlasting in rivers. It is an easy-to-
operate strategy for power performance improvement and organics
and nitrogen removal. In lakes or ponds where the water flows at rel-
ative low velocity or even maintains static, simple constructions
could be used to enable water flows, which would accelerate atmo-
spheric reoxygenation and accordingly increase the performance of
SMFCs. Generally, the overlying water flow and hydraulic-driven
cathode rotating are promising strategies for performance improve-
ment in SMFCs.
4. Conclusions
Cathode rotating in SMFCs could be cost-effectively accomplished
with hydraulic energy as the alternative driving force. Deteriorated
cathode potential and power generation under static condition in
SMFC-C due to the reduced oxygen availability and mass transfer rate
was improved by the overlying water flow. It was also concluded that
ORR in SMFC-R was mainly occurred at the cathode exposed to the air
rather than that submerged below the overlying water, greatly reducing
mass transport losses even under static condition. Cathode rotating
could further improve the power performance in SMFC-R due to the ac-
celerated mass transfer rate. Identical anode performance was obtained
in both SMFCs under different conditions, which was not an influencing
factor leading to the different power performance of SMFCs. However,
in this work, we mainly focused on the strategies for power perfor-
mance improvement and did not test organic matter or nutrients re-
moval, which is worthy to be further investigated. Generally, the
overlying water flow and hydraulic-driven cathode rotating are practi-
cal strategies for power performance improvement, pushing SMFCs
technology forward field applications in remote areas.
Acknowledgements
This research was financially supported by the National Science
Foundation of China (No. 51525805), and by the talents program of
Xihua University.
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