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energies
Review
Applications of Emerging Bioelectrochemical
Technologies in Agricultural Systems:
A Current Review
Simeng Li 1, * , Gang Chen 1and Aavudai Anandhi 2
1Department of Civil and Environmental Engineering, FAMU-FSU College of Engineering,
2525 Pottsdamer Street, Tallahassee, FL 32310-6046, USA; gchen@eng.famu.fsu.edu
2
Biological Systems Engineering, Florida Agricultural and Mechanical University, Tallahassee, FL 32307, USA;
anandhi@famu.edu
*Correspondence: sl16b@my.fsu.edu; Tel.: +1-850-645-0126
Received: 10 October 2018; Accepted: 26 October 2018; Published: 29 October 2018
Abstract:
Background: Bioelectrochemical systems (BESs) are emerging energy-effective and
environment-friendly technologies. Different applications of BESs are able to effectively minimize
wastes and treat wastewater while simultaneously recovering electricity, biohydrogen and other
value-added chemicals via specific redox reactions. Although there are many studies that have greatly
advanced the performance of BESs over the last decade, research and reviews on agriculture-relevant
applications of BESs are very limited. Considering the increasing demand for food, energy and
water due to human population expansion, novel technologies are urgently needed to promote
productivity and sustainability in agriculture. Methodology: This review study is based on an
extensive literature search regarding agriculture-related BES studies mainly in the last decades
(i.e., 2009–2018). The databases used in this review study include Scopus, Google Scholar and Web of
Science. The current and future applications of bioelectrochemical technologies in agriculture have
been discussed. Findings/Conclusions: BESs have the potential to recover considerable amounts
of electric power and energy chemicals from agricultural wastes and wastewater. The recovered
energy can be used to reduce the energy input into agricultural systems. Other resources and
value-added chemicals such as biofuels, plant nutrients and irrigation water can also be produced in
BESs. In addition, BESs may replace unsustainable batteries to power remote sensors or be designed
as biosensors for agricultural monitoring. The possible applications to produce food without sunlight
and remediate contaminated soils using BESs have also been discussed. At the same time, agricultural
wastes can also be processed into construction materials or biochar electrodes/electrocatalysts for
reducing the high costs of current BESs. Future studies should evaluate the long-term performance
and stability of on-farm BES applications.
Keywords:
bioelectrochemical system; agriculture sustainability; electricity generation; resource
recovery; desalination; agricultural monitoring; biochar
1. Introduction
Energy is an important and necessary input for today’s increasingly mechanized agriculture.
Farm production, for both crop and animal products, requires direct use of energy as fuel or electricity
to operate diverse farm machinery and equipment and maintain other agricultural activities (Table 1),
and also indirect use of energy due to the consumption of fertilizers and pesticides. The supply and
demand of energy in agricultural systems can significantly impact the profitability of agriculture [
1
].
At the same time, excessive use of fossil fuels, fertilizers and pesticides, etc. in crop production, as well
as the misuse of antibiotics in livestock production, can result in many environmental problems such as
Energies 2018,11, 2951; doi:10.3390/en11112951 www.mdpi.com/journal/energies
Energies 2018,11, 2951 2 of 21
greenhouse gas emission and water body contamination [
2
–
4
]. In addition, many agricultural systems
produce a vast amount of different waste materials that need to be appropriately treated or disposed [
5
].
These agricultural wastes, such as stover and livestock manure, usually contain large amounts of
microbially degradable organic matter [
6
]. In response to the call for improving sustainability in
agriculture, a variety of environment-friendly technologies that utilize agricultural wastes for energy
production or resource recovery have been recently developed and applied in agricultural systems,
among which bioelectrochemical systems (BESs) seems to be the most promising [7].
Table 1. Direct energy uses in agricultural production.
Uses of Energy Types of Energy
Operating agricultural machinery and large trucks Diesel
Operating small vehicles Gasoline
Irrigation; crop processing; heating/cooling; animal
waste treatment
Diesel; natural gas; liquified petroleum gas; electricity
Power for farm houses and facilities Electricity
As hybrid systems of microbiology and electrochemistry, BESs are able to produce electrical
energy or various value-added chemicals via different microorganism-catalyzing redox reactions [
8
].
Like in other types of electrochemical systems (e.g., batteries), electricity is automatically generated
when the redox potential of the reduction half-reaction on the cathode is larger than that of the
oxidation half-reaction on the anode. Otherwise, the flow of electrons can be driven by external power
in order to impel desired redox reactions for resource recovery [
7
]. Because BESs are able to use
diverse biodegradable organics as electron donors, simultaneous degradation of these organics can be
effectively achieved as well [
9
]. Depending on the diverse end objectives, BESs generally vary greatly
in reactor configurations, dimensions, substrates, bacterial communities, etc. [
7
]. In spite of the various
differences, BESs are usually classified according to their application purposes (Figure 1) and can be
divided into microbial fuel cells (MFCs), microbial electrolysis cells (MECs), microbial electrosynthesis
(MESs), microbial desalination cells (MDCs), microbial solar cells (MSCs), and enzymatic biofuel cells
(EFCs) [
8
]. The components, mechanisms and applications of these different types of BESs are briefly
discussed in the next section.
Over the last decade, considerable efforts have been made to advance the performance and
applicability of emerging BESs focusing on treating domestic and industrial wastewater, and a lot of
significant progress has been achieved [
9
]. However, in comparison, applications of BESs in agriculture
have received much less attention. There is also a lack of state-of-the-art reviews on the applications of
BESs in agricultural systems. Therefore, this article presents a critical review on the past studies of
BESs with an emphasis on the applications related to agriculture. Moreover, with the discussion on the
current and future applications of different BESs in agricultural systems, this article also aims to draw
a blueprint of future sustainable agricultural systems tackling the nexus of food, energy and water
using emerging BES technologies. The rest of the paper is structured as follows: Section 2describes
the methodology used for this review study; Section 3provides brief introductions of different types
of BESs; Section 4summarizes diverse agricultural applications of BESs that are currently available;
Section 5discusses various agricultural applications of BESs that are potential in the future.
Energies 2018,11, 2951 3 of 21
Energies 2018, 11, x FOR PEER REVIEW 3 of 20
Figure 1. Different bioelectrochemical systems (BESs) classified by application purposes.
2. Methodology
This review study is based on an extensive literature search regarding agriculture-related BES
studies mainly in the last decade (i.e., 2009–2018) (Figure 2). Three potent databases, Scopus, Google
Scholar and Web of Science, were utilized to locate and access the literature, respectively.
Appropriate search terms and time ranges were defined within each database. For example, in order
to find literature on the applications of MFC in agriculture, a general search term “microbial fuel cell
AND agriculture” was first used. Afterwards, more specific search terms such as “microbial fuel cell
AND animal wastewater” were also used. The process was repeated with various relevant search
terms until no additional studies were found. The time range was first set for 2009–2018. However,
under situations where the number of studies returned from the search was small, the time range
was then extended for 1999–2018. The cut-off date for publications that were included in this review
study was 31 September 2018. The search results were carefully selected because many of the studies
were either unable to provide sufficient information or the information was irrelevant. In addition,
only peer-reviewed literature was selected for this work. The discussion of current applications of
BESs in agriculture were completely based on the information and data collected from the literature.
Whereas, agricultural applications of BESs in the future were discussed according to both peer-
reviewed literature and science-based reasoning. Whenever necessary, relevant data that were
presented graphically were extracted using free-access DataThief III.
Figure 1. Different bioelectrochemical systems (BESs) classified by application purposes.
2. Methodology
This review study is based on an extensive literature search regarding agriculture-related BES
studies mainly in the last decade (i.e., 2009–2018) (Figure 2). Three potent databases, Scopus, Google
Scholar and Web of Science, were utilized to locate and access the literature, respectively. Appropriate
search terms and time ranges were defined within each database. For example, in order to find literature
on the applications of MFC in agriculture, a general search term “microbial fuel cell AND agriculture”
was first used. Afterwards, more specific search terms such as “microbial fuel cell AND animal
wastewater” were also used. The process was repeated with various relevant search terms until no
additional studies were found. The time range was first set for 2009–2018. However, under situations
where the number of studies returned from the search was small, the time range was then extended for
1999–2018. The cut-off date for publications that were included in this review study was 31 September
2018. The search results were carefully selected because many of the studies were either unable to
provide sufficient information or the information was irrelevant. In addition, only peer-reviewed
literature was selected for this work. The discussion of current applications of BESs in agriculture were
completely based on the information and data collected from the literature. Whereas, agricultural
applications of BESs in the future were discussed according to both peer-reviewed literature and
Energies 2018,11, 2951 4 of 21
science-based reasoning. Whenever necessary, relevant data that were presented graphically were
extracted using free-access DataThief III.
Energies 2018, 11, x FOR PEER REVIEW 4 of 20
Figure 2. Rationale of methodology.
3. Types of BESs
3.1. Microbial Fuel Cells (MFCs)
MFCs (Figure 1a) are the most fundamental BESs and have been extensively investigated
towards real-world applications [10,11]. With electrochemically active bacteria (i.e., exoelectrogens)
such as Geobacter sulfurreducens and Shewanelle putrefaciens on the anode, MFCs are able to generate
electrical energy directly from a broad range of biodegradable organics through different redox
reactions on the electrodes [12]. In MFCs, the organics in the anode compartment serve as electron
donors when they are consumed by exoelectrogens, which produce extracellular electrons that can
be collected from the anode. Through an external circuit, the electrons flow to the cathode, thus
forming an electric current that can be harnessed for immediate usage or stored for later [8]. The
development of air-cathode MFCs has made this technology more feasible to treat wastewater and
harvest electricity in practice [13]. Many studies, including some pilot studies [13–15], have reported
considerable electric power generation from domestic wastewater [16], industrial wastewater [9],
landfill leachate [12], and swine wastewater [17], etc. However, the high cost of the electrodes and
the diminished power at larger scales are the two main factors limiting the commercial applications
of larger-scale MFCs [13].
3.2. Microbial Electrolysis Cells (MECs)
Adapted from MFCs, MECs are capable of producing hydrogen gas (H2), methane (CH4) or other
value-added chemicals for indirect energy usage and storage [8]. Theoretically, MECs are able to
produce any value-added chemicals regardless of the redox potential differences on the electrodes
[18]. The thermodynamic barriers for accomplishing required redox reactions are resolved by driving
the electron flow with external electric power (Figure 1b). In order to maximize the usage efficiency
of electrons for the production of desired products, the cathode compartment needs to be maintained
as anaerobic or anoxic. Among the products that can be produced in MECs, H2 has demonstrated
very promising commercialization potential as a renewable energy, considering the convenience for
storage and transportation, as well as the rapidly increasing market demand of H2 [19]. The system
efficiency of MECs is significantly higher than that of other BESs [18], and therefore, more and more
research attention has been focused on producing H2 in MECs using a variety of wastes and
wastewater [20–23]. During the recent years, remarkable advances in MEC-based H2 production have
been reported, with H2 yield (i.e., moles of produced hydrogen per moles of consumed substrate, or
Figure 2. Rationale of methodology.
3. Types of BESs
3.1. Microbial Fuel Cells (MFCs)
MFCs (Figure 1a) are the most fundamental BESs and have been extensively investigated towards
real-world applications [
10
,
11
]. With electrochemically active bacteria (i.e., exoelectrogens) such as
Geobacter sulfurreducens and Shewanelle putrefaciens on the anode, MFCs are able to generate electrical
energy directly from a broad range of biodegradable organics through different redox reactions on
the electrodes [
12
]. In MFCs, the organics in the anode compartment serve as electron donors when
they are consumed by exoelectrogens, which produce extracellular electrons that can be collected
from the anode. Through an external circuit, the electrons flow to the cathode, thus forming an
electric current that can be harnessed for immediate usage or stored for later [
8
]. The development of
air-cathode MFCs has made this technology more feasible to treat wastewater and harvest electricity in
practice [
13
]. Many studies, including some pilot studies [
13
–
15
], have reported considerable electric
power generation from domestic wastewater [
16
], industrial wastewater [
9
], landfill leachate [
12
],
and swine wastewater [
17
], etc. However, the high cost of the electrodes and the diminished power at
larger scales are the two main factors limiting the commercial applications of larger-scale MFCs [13].
3.2. Microbial Electrolysis Cells (MECs)
Adapted from MFCs, MECs are capable of producing hydrogen gas (H
2
), methane (CH
4
) or other
value-added chemicals for indirect energy usage and storage [
8
]. Theoretically, MECs are able to
produce any value-added chemicals regardless of the redox potential differences on the electrodes [
18
].
The thermodynamic barriers for accomplishing required redox reactions are resolved by driving the
electron flow with external electric power (Figure 1b). In order to maximize the usage efficiency of
electrons for the production of desired products, the cathode compartment needs to be maintained
as anaerobic or anoxic. Among the products that can be produced in MECs, H
2
has demonstrated
very promising commercialization potential as a renewable energy, considering the convenience for
storage and transportation, as well as the rapidly increasing market demand of H
2
[
19
]. The system
efficiency of MECs is significantly higher than that of other BESs [
18
], and therefore, more and
Energies 2018,11, 2951 5 of 21
more research attention has been focused on producing H
2
in MECs using a variety of wastes and
wastewater [
20
–
23
]. During the recent years, remarkable advances in MEC-based H
2
production have
been reported, with H
2
yield (i.e., moles of produced hydrogen per moles of consumed substrate,
or mass of produced hydrogen per mass of consumed substrate) raised from less than 50% to nearly
100%, and H
2
production rates elevated from below 0.1 m
3
H
2
/m
3
reactor/day to as high as 50 m
3
H2/m3reactor/day [18].
3.3. Microbial Electrosynthesis (MESs)
As a novel perspective of BESs, MES (Figure 1c) is a form of microbial electrocatalysis
that can produce value-added products (e.g., acetate, butyrate, ethanol, and biodiesel, etc.) by
electric power-driven reduction of CO
2
and other organics at the biocathode using microorganisms
as a biocatalyst [
24
]. Given appropriate biocatalysts, electron acceptors and redox mediators,
the value-added products produced in MESs can be highly specific [
25
]. Notably, depending on
the feeding substrates, various industrially relevant products such as bioethanol, biofuel and bulk
chemicals can also be produced via oxidation reactions at the anode in MESs [
24
]. The feeds suitable
for MESs are similar to those reported for MFCs, but external electric power is utilized in MESs to
generate organics [
26
]. As such, the processes in MESs are opposite to those employed in MFCs,
and energy is stored in covalent chemical bonds instead. At the same time, it should also be noted that
MESs are related to (but different from) MECs, in which the external electric power provides additional
electrical potential to make it sufficient for the reduction reactions at the cathode, e.g., reduction of
H
+
to H
2
[
27
]. MESs have a significant diversity of applications, as the various end products include
but are not limited to different types of biofuels [
28
], industrially relevant chemicals [
29
] and drug
precursors [
30
], etc. Therefore, many researchers believe that the role of MESs in future bioproduction
will be increasingly important [30].
3.4. Microbial Desalination Cells (MDCs)
MDCs have been modified from MFCs to cut down the high energy demand of commonly used
desalination technologies (e.g., reverse osmosis, electrodialysis and mechanical vapor compression,
etc.) [
31
]. In MDCs, a desalination compartment equipped with a cation exchange membrane (CEM)
and an anion exchange membrane (AEM) is inserted in between the anode and cathode compartments
(Figure 1d). Driven by the electrochemical potential differences between the electrodes, the cations and
anions flow through the CEM and AEM into the cathode and anode compartments, respectively [32].
As a result, the saltwater is desalinated with the losses of ions. At the same time, the electrical
energy recovered from the organics in the anode compartment can be utilized or stored elsewhere.
High desalination efficiency of 90%, together with a maximum power density of 31 W/m
3
, has been
observed with the use of acetate as an electron donor and ferricyanide as an electron acceptor [
31
].
Further studies have shown that domestic wastewater as an electron donor and sparged air as an
electron acceptor could also achieve considerable salinity removal of over 60% [
33
]. Due to the
advantages of treating wastewater and desalinating saltwater simultaneously in a single device while
retrieving electric power from these processes, MDCs have been widely considered as a promising
energy-efficient technology to address emerging challenges, including saltwater and brackish water
desalination, value-added chemical production, groundwater remediation, wastewater treatment,
and energy recovery [31,34–36].
3.5. Microbial Solar Cells (MSCs)
MSCs are BESs that can recover in-situ bioelectricity or value-added chemicals by integrating
photosynthesis and exoelectrogenesis [
37
]. MSCs (Figure 1e) use photosynthetic organisms such
as photoautotrophic microorganisms or higher plants to convert solar energy to chemical energy
in organic matter, which is further utilized by MFC components to generate electricity. The key
process in an MSC is the transport of the organic matter produced from photosynthesis to the anode
Energies 2018,11, 2951 6 of 21
compartment. There are generally three modes of transfer, i.e., through the rhizodeposition of a high
plant, through the diffusion of a phototrophic biofilm, or through the pumping for translocation from a
photobioreactor or coastal marine ecosystem [
37
]. Among the various types of MSCs, those integrated
with living higher plants (a.k.a., plant microbial fuel cells (PMFC)) have demonstrated the most effective
power generation as high as 1000 GJ/ha/year (i.e., 3.2 W/m
2
), as estimated by recent studies [
37
–
39
].
The power generation from PMFCs has been found directly related to the availability of rhizodeposits
for anodic oxidation reactions [
7
]. Unlike conventional solar cells, MSCs are able to generate not only
electricity, but also a great diversity of value-added chemicals [
40
]. Benefitting from the continuously
growing population of microorganisms carrying out the photosynthetic and electrochemical reactions,
MSCs are self-repairing systems with a longer lifetime and lower maintenance [
37
]. The applications of
MSCs are broad and promising because they are compatible with many different systems as sustainable
and eco-friendly energy suppliers or biosynthesis reactors [41].
3.6. Enzymatic Biofuel Cells (EFCs)
EFCs utilize specific oxidoreductase enzymes as electrocatalysts to convert the chemical energy
stored in organic matter into directly usable electrical energy with the oxidation reactions at the
anode and reduction reactions at the cathode (Figure 1f). In early EFCs, enzymes were used in the
electrolyte suspension but the systems were plagued by low performance and stability [
42
]. Recent
studies have developed different techniques to immobilize and stabilize enzymes at the electrode
surface [
43
]. For example, crosslinking redox hydrogels, as well as sandwich and encapsulation
techniques, have been used to entrap enzymes while allowing for uninterrupted transport of organic
matter within the compartments [
44
]. At the same time, to improve the system stability of EFCs,
biocatalysts from thermophilic microorganisms have been widely investigated considering their
better thermal stability under higher operation temperatures [45–47]. With the rapid development in
recent years, EFCs have been applied to power biosensors and portable devices [
46
,
48
–
50
], as well as
implantable systems [
51
–
53
]. Researchers have also been actively excavating the potential of EFCs for
energy conversion and storage from different sources [46].
4. Current Applications of BESs in Agriculture
4.1. Direct Generation of Electric Power
Among the different BESs, MFCs have been widely studied in many countries to treat a
diversity of agricultural wastes and animal wastewater while simultaneously generating sustainable
bioelectricity that can be directly utilized as on-farm electric power supply [
17
,
54
–
57
]. The resulting
electric power varied depending on the type and concentration of feed, as well as the type of MFC
reactor (Table 2). For example, with swine wastewater containing 8320
±
190 mg/L of soluble
chemical oxygen demand (SCOD), Min et al. [
17
] obtained a maximum power density of 45 mW/m
2
using a two-chamber MFC with an aqueous cathode but a significantly higher maximum power
density of 261 mW/m
2
using a single-chamber air-cathode MFC. However, a later study using
the same type of MFC (i.e., single-chamber air-cathode) to treat less concentrated swine wastewater
(1820 ±83 mg SCOD/L)
only achieved a relatively lower maximum power density of 205 mW/m
2
[
56
].
In addition, lignocellulosic biomass such as corn stover and wheat straw has also been investigated
as possible feed for MFCs [
58
–
60
]. For instance, Wang et al. [
58
] used both raw and steam-exploded
corn stover to feed single-chamber air-cathode MFCs and observed considerable maximum power
densities of 296 and 343 mW/m
2
, respectively. In addition, wastewater from agriculture-relevant
industries, e.g., rice mill wastewater [
61
] and food-processing wastewater [
62
], has also been identified
as potential feed for effective electricity generation in MFCs. However, despite the continuous progress
in using agricultural wastes and wastewater to feed MFCs, the electricity production with these
applications is often challenged by the occurrence of other microbial processes such as methanogenesis
(i.e., the generation of methane) and ammonification (i.e., the conversion of organic nitrogen to
Energies 2018,11, 2951 7 of 21
ammonia) [
17
,
55
]. In MFCs, the reduction of carbon dioxide to methane in the anode compartment
consumes electrons, thus decreasing the Coulombic efficiency and lowering the power generation [
10
].
Also, high concentrations of ammonia are toxic to most exoelectrogens that power MFCs [
63
]. Therefore,
in order to maximize the electricity recovery from agricultural wastes and wastewater, future efforts
need to be focused on minimizing the negative impacts of methanogenesis and ammonification on
MFC performance.
MSCs, or more specifically, PMFCs, [
64
] have also attracted research attention in the recent
years for their potential to generate electricity from the rhizodeposits, i.e., organic compounds
(e.g., sugars, organic acids, polymeric carbohydrates, enzymes, and cellular debris, etc.) excreted
from plant roots [
37
]. Some MSC studies have integrated the MFC anode into the plant-growing
soil, where the rhizodeposits from the plants and organic matter from the soil were available for
electricity production [
65
–
67
]. The electricity production by a PMFC in practice has been conservatively
estimated to be 21 GJ ha
−1
year
−1
(equivalent to 67 mW/m
2
) [
68
]. Significantly higher power
generation of 300 mW/m
2
has been observed in laboratory-scale experiments harvesting electricity
from rhizodeposits of rice plants [
67
]. A long-term PMFC study conducted using S. anglica generated
an average power generation of 50 mW/m
2
[
64
], in which it is possible to be greatly improved by
a change of the ion transport direction within the bioelectrochemical reactor [
69
]. To advance the
research and practical applications of PMFCs, the principal processes must be further understood.
Mechanistic models also need to be established to optimize the design of system constituents and
operation conditions [37].
Table 2.
Electric power generation in microbial fuel cells (MFCs) using different types of agricultural
wastes/wastewater.
Type of Feed Concentration
(mg SCOD/L) Type of MFC Power Generation
(mW/m2)Reference
Swine wastewater 8320 Two-chamber; aqueous cathode 45 [17]
Swine wastewater 8320 Single-chamber; air-cathode 261 [17]
Swine wastewater 1820 Single-chamber; air-cathode 205 [56]
Dairy manure wastewater 450 Single-chamber; air-cathode 189 [70]
Cattle manure leachate 4000 Two-chamber; air-cathode 216 [71]
Cattle manure slurry 2500 Cassette-electrode; air-cathode 163 [72]
Raw corn stover 1000 Single-chamber; air-cathode 296 [58]
Steam-exploded Corn stover 1000 Single-chamber; air-cathode 343 [58]
Steam-exploded Corn stover 1000 Single-chamber; air-cathode 371 [59]
Wheat straw 2000 Two-chamber; aqueous cathode 123 [60]
4.2. Production of Biohydrogen
Many different types of agricultural wastewater such as dairy manure slurry [
73
],
swine wastewater [
74
] and fermentation effluent [
75
] have been used for the production of biohydrogen
in MECs (Table 3). Comparing with other biohydrogen technologies such as anaerobic digestion and
photobiological processes, MECs have demonstrated better performance in producing H
2
from more
diverse substrates because of its ability to overcome thermodynamic limitations [
18
,
76
]. However,
the performance of MECs, in terms of the H
2
production rate and H
2
yield, varies when different
substrates were used for the conversion [
77
]. Highest H
2
production rate up to 50 m
3
/m
3
/day and
H
2
yield of nearly 100% have been reported for MECs utilizing readily biodegradable organics such
as acetate and other fermentation products from anaerobic digesters [
18
]. For the same MEC system
using the same substrate, the application of a higher external voltage typically results in higher H
2
production rate and H
2
yield because of the improved electron transfer towards the cathode driven by
the increased voltage. However, a higher external voltage typically decreases the energy efficiency
because there is a need for more energy input. It has been reported that the H
2
production and energy
efficiency could be balanced with an optimal external voltage of 0.6–0.8 V [
76
]. At the same time,
external voltages supplied by renewable electric power from MFCs and other sustainable power
sources can also be utilized to operate MECs [78].
Energies 2018,11, 2951 8 of 21
Anaerobic digesters are fermentation facilities commonly used for the minimization of agricultural
wastes and recovery of useful biogases such as H
2
and CH
4
[
79
]. The integration of MECs with
anaerobic digesters have achieved enhanced H
2
production rate and yield [
18
]. The fermentation in
anaerobic digesters can break down large-molecular-weight carbohydrates into small-molecular-weight
metabolites that are more readily biodegradable for MECs. The CO
2
produced during the fermentation
processes can be recirculated through electrolytes for pH buffering [
80
]. With the substrates generated
from fermentation, MECs can be configured to produce high-purity H
2
under variable operational
conditions [
81
]. So far, using integrated systems, the highest H
2
production rate of 189 m
3
/m
3
/day has
been reported by Lo et al., which is nearly four times the H
2
production rate using MECs alone [
82
].
The integration of MECs also completes the oxidation of organics into CO
2
which fermentation alone
cannot achieve. The integrated systems were capable of producing H
2
effectively from lignocellulosic
materials that are traditionally considered as recalcitrant agricultural wastes, including corn stover,
sugar beet, plant leaves, and corn stalk, etc. [
83
–
86
]. When combined with fermentation, the average
overall increases of H
2
production rate and yield were 148% (ranging from 42 to 538%) and 225%
(ranging from 2 to 400%), respectively [
18
]. The matching between fermentation and electrohydrogenesis
rates is the key to further improvement in the system performance, which can be achieved through
specially designed feeding strategies or novel stepwise processes [
76
]. Although long-term pilot studies
of MECs have been conducted, larger-scale MECs have not been built up yet, mainly due to economic
concerns from the expensive costs of electrodes and external energy inputs [
87
–
89
]. In practice, relatively
more inexpensive renewable power sources for H
2
production in MECs could be wind, geothermal and
hydropower, etc.
Table 3.
H
2
production in microbial electrolysis cells (MECs) from different types of agricultural
wastes/wastewater.
Type of Feed MEC Volume
(mL)
Applied
Voltage (V)
H2Production
Rate (m3/m3/day)
Overall H2
Yield (%)
Energy
Efficiency (%) Reference
Corn stalk 64 0.8 3.43 64 166 [90]
Wheat straw 210 0.7 0.61 64 NA [91]
Swine wastewater 28 0.5 0.9–1.0 17–28 58–74 [92]
Potato wastewater 28 0.9 0.74 73 NA [70]
Switchgrass wastewater 16 1.0 4.3 50–76 149–175 [93]
Fermentation effluent 26 0.6 2.11 96 287 [94]
Fermentation effluent 64 0.9 4.55 51 185 [95]
4.3. Production of Biofuels and Other Value-Added Chemicals
Besides direct energy recovery in the form of electricity using MFCs and H
2
using MECs,
organic-rich agricultural wastes and wastewater have also been used for the production of biofuels
and other value-added chemicals in MESs [
24
]. With the use of CO
2
and clean water, MESs are
capable of converting agricultural and forestry residues (e.g., corn stalk, stover, wood, grass, leaves,
immature cereal, etc.) into syngas [
29
], H
2
[
96
], CH
4
[
97
], formic acid [
98
], ethylene [
24
], methanol [
99
],
dimethyl ether [
100
], urea [
7
], succinic acid [
101
], etc. Through mineralization reactions, CO
2
can
also be synthesized into precursors of polymers and carbonates for construction applications [
102
].
With appropriate redox reactions at the anode and cathode, as well as adequate external input to
balance the potential difference, MESs are able to produce many other value-added chemicals including
biofuels such as bioethanol and biodiesel [
7
,
103
]. Sadhukhan et al. have summarized the equations and
Gibbs free energies of 63 anode reactions, 72 cathode reactions and 9 metabolic pathways in MESs that
could be used to assess the technical feasibility or thermodynamic spontaneity of resource recovery
from wastes and wastewater and combinations of redox reactions [24].
Agricultural residues are abundant and renewable organic feeds for MESs. However,
most agricultural biomass are lignocellulosic, meaning a complex mixture of structural polysaccharides
such as cellulose and hemicellulose encased by lignin (main constituent of plant cell walls) that
is recalcitrant to microbial oxidation [
104
]. Therefore, oftentimes agricultural residues must be
Energies 2018,11, 2951 9 of 21
fractionated or pretreated to derive monosaccharides or other small-molecular-weight compounds
before they can be utilized by microorganisms in MESs to produce value-added chemicals [
29
]. At the
same time, cellulose and hemicellulose can be recovered during the pretreatment and be further
processed to produce many different industrial chemicals such as xylite, L-arabinose, furan resins,
and nylons, etc. [
24
]. Lignin can also be recovered to produce wood adhesives, epoxy resins,
fuel additives, binders, carbon fiber, and precursors for pharmaceuticals and fragrances [
24
].
Low-strength agricultural wastewater processed from wheat bran, sugar cane bagasse, coffee husk,
pineapple waste, or carrot, etc., as well as stillage streams from on-farm biorefinery processes and
fermentation effluent, are suitable substrates in MESs [
96
]. The biodegradability of the substrate decides
the efficiency of usage by the microorganism. The microbial conversion of lignocellulosic biomass
typically undergoes hydrolysis, acidogenesis, acetogenesis, and methanogenesis chronologically [
12
],
among which acetogenesis is able to match well with the bioelectrochemical processes and optimize
the electron generation at the anode. On the cathode side, electrons donated from the organics can
reduce CO
2
to produce targeted organic chemicals. Over the last few years, BES technologies such as
MECs and MESs have also been developed to recover metals from wastewater in a less destructive
and disruptive manor [
7
]. Comparing to conventional metal recovery technologies using chemical
precipitation, BES technologies, besides their significant metal selectivity, can greatly improve the
efficacy and reduce costs from startup, operation and maintenance [
105
]. In addition, these BES
technologies can be integrated with diverse agricultural and industrial systems for selective syntheses
of value-added products [24], thus increasing the overall sustainability and economic significance.
4.4. Removal and Recovery of Nutrients
Agricultural wastewater such as animal wastewater is abundant in recyclable nutrients. Animal
wastewater with high concentrations (>500 mg/L) of organic nitrogen (N) and ammonia (NH
3
) is
usually inhibitory to anode-respiring activities and is undesirable for wastewater treatment [
106
],
but with appropriate pretreatment and enhanced reactor designs, the removal and recovery of N
in forms of NH
3
, NH
4+
and NO
3−
from N-rich wastewater streams can be effectively achieved
with the applications of BES technologies [
7
,
107
]. Using recently developed denitrifying biocathode
in MFCs or MECs, the removal of NO
3−
can be easily realized by using NO
3−
as the electron
acceptor at the electron-donating cathode to generate N
2
(i.e., bioelectrochemical denitrification),
which is accompanied with simultaneous generation of electricity or H
2
, respectively [
108
]. However,
the removal of NH
3
or NH
4+
in BESs is mainly through conventional physical separation or nitrification
because the thermodynamic kinetics for anaerobic ammonium oxidation (i.e., Anammox) process
are very slow [
109
]. Therefore, aerobic process has been incorporated into MFC or MEC systems for
nitrification that converts NH
4+
to NO
3−
, followed by anaerobic denitrification that reduces NO
3−
into N
2
at the biocathode [
110
]. In addition, BESs integrated with algae growth has enhanced the
efficiency of N removal and achieved high nitrogen removals of over 87%, and is greatly attributed to
the assimilation of nutrients through photosynthetic metabolisms [
111
]. Recent BES studies have also
discovered that bioelectrochemical reactions can drive NH
3
or NH
4+
to be separated from the anolyte
and migrate/diffuse into the catholyte across the cation exchange membrane (CEM), which led to the
discovery of NH3recovery using BES technologies [112].
In agricultural systems, recovering nutrients from wastewater is more sustainable than removing
them, as the recovered nutrients can be used to fertilize farmlands that are suffering from nutrient
depletion. N is one of the most important and necessary plant nutrients [
4
]. N recovery in BESs
is mainly through NH
3
recovery driven by the generated electric current, although N can also
be recovered through assimilation and stored in algal cells using algae-containing systems [
112
].
The NH
3
in the anolyte can transport via both migration and diffusion across the CEM to the catholyte,
where NH
3
-N up to several grams per liter can be accumulated [
113
]. The NH
3
recovery efficiency
can be nearly 100% in some BESs [
107
]. The high pH of the catholyte can stimulate the generation
of NH
3
, which can be stripped from the catholyte and captured in an acid solution for producing
Energies 2018,11, 2951 10 of 21
N nutrients later. Similar to MFCs which generate electricity while recovering NH
3
, MECs can
produce H
2
simultaneously. A recent study reported up to 96% recovery of NH
3
with considerable H
2
generation using MECs that were fed with wastewater containing high concentrations (approximately
1000 mg/L) of NH
3
[
113
]. The rate of N recovery is similar to that in conventional biological processes
(e.g., nitrification and denitrification), which is probably because of the similar microbial redox
processes involved for the conversions [112].
In addition to N, other important plant nutrients such as phosphorus (P) and potassium (K) can
also be recovered from agricultural wastewater in BESs, depending on the richness of the target nutrient
in the raw wastewater [
7
]. For example, high recovery efficiencies of P ranging from 58 to 92% have
been observed in MFCs integrated with algal photosynthesis [
112
]. At the same time, BES operation
can also create a high-pH zone near the cathode to improve struvite precipitation [
114
]. The main
advantages of using BESs for nutrient recovery include the lower demand for input of organics,
simultaneous energy generation (either as electricity or H
2
), less negative impacts on environment,
and good compatibility with other systems, etc.
4.5. Treatment of Agricultural Wastes and Wastewater
Most agricultural wastes and wastewater, especially highly concentrated animal wastes and
wastewater, need to be treated before they can be disposed/discharged or merged into domestic
wastewater streams for further treatment in wastewater treatment plants (WWTPs) [
57
]. Solid animal
wastes are usually handled by composting or anaerobic digestion, but they can also be effectively
treated in BESs to retrieve resources or energy as a bonus [
10
]. The removal of chemical oxygen
demand (COD) is an indicator for the removal of organics during wastewater treatment. Considerable
COD removal as high as 98% in BESs treating different types of agricultural wastewater has been
widely reported (Table 4). BESs have also demonstrated effectiveness in pretreating high-strength
lignocellulosic biomass hydrolytes. For example, using a single-chamber air-cathode MFC with
non-catalyzed electrodes, Mohan et al. [
115
] removed 63% of the high influent COD (52 g/L) derived
from the hydrolyte of composite vegetables. At the same time, 57 mW/m
2
of electric power was
able to be recovered. In another study, by integrating dark fermentation and single-chamber MECs,
Li et al.
[
90
] reported a considerable H
2
generation of 3.43 m
3
/m
3
/day with 44% of COD removed
from the original 20 g/L of COD which resulted from corn stalk. These results showed that BESs can
serve as potential pretreatment units for agricultural wastes and wastewater. Each type of BESs can
be stacked for enhanced overall performance. In addition, MFCs can be used to supply the external
electric power required for other BESs such as MECs and MESs [
8
], thus reducing the energy demand
for waste and wastewater treatment while diversifying the added values from resource recovery.
Table 4.
Performance comparisons of bioelectrochemical systems (BESs) for treating agricultural wastes/
wastewater: MFC—microbial fuel cell; MEC—microbial electrolysis cell; MES—microbial electrosynthesis.
BES Type Waste/Wastewater Type Original COD (mg/L) COD Removal (%) Recovered Energy/Resources Reference
MFC Cattle manure slurry 2500 39 Electric power (163 mW/m2)[72]
MFC Swine wastewater 8320 83 Electric power (261 mW/m2)[17]
MFC Corn stover hydrolysate 1000 70 Electric power (867 mW/m2)[59]
MFC Composite vegetables 52,000 63 Electric power (57 mW/m2)[115]
MFC Starch processing wastewater 4852 98 Electric power (239 mW/m2)[116]
MEC Swine wastewater 2000 75 Bio-H2(1.00 m3/m3/day) [92]
MEC Corn stalk 20,000 44 Bio- H2(3.43 m3/m3/day) [90]
MEC Animal urine 1360 46 Bio-H2(32.0 m3/m3/day) [117]
MES Lignocellulosic biomass 10,000 70 Butanol (0.88 g/L/day)
Ethanol (1.99 g/L/day) [118]
4.6. Water Desalination for Irrigation
Agricultural activities consume a great amount of water, accounting for approximately 70% of
the total water usage globally [
119
]. At the same time, the continuing world human population
expansion and deteriorating global warming have been adding more severity to the issue of water
Energies 2018,11, 2951 11 of 21
scarcity [
120
]. Although desalination technologies such as reverse osmosis, thermal desalination and
electrodialysis have been maturely developed to supply high-quality freshwater in areas sufficient in
brackish water and seawater but limited for freshwater sources, these technologies are energy-intensive
and unsustainable [
31
]. MDCs are sustainable BESs specifically designed for low-cost desalination,
which can overcome the drawbacks of the existing technologies and bring more economic, energy
and environmental benefits to the desalination process [
32
]. Considering the low desalination rate
using MDCs, most MDC systems today are applied for pre-desalination of seawater or desalination
of brackish water (with less salinity than seawater) [
32
]. In many arid areas, freshwater shortage
has forced farmers to use brackish groundwater for irrigation, which may temporarily relieve the
freshwater stress but result in long-term issues such as accumulation of ions toxic to plants and increase
of soil salinity [
121
]. High soil salinity can further weaken plants’ ability to uptake water because of its
resulting high osmotic potentials [
121
]. Therefore, in order to cause less harm to soil property and crop
growth, the salinity of irrigation water should be ensured below 450 mg/L of total dissolved solids
(TDS) [122].
Current MDCs have demonstrated solid abilities to desalinate brackish water to meet the standard
of 450 mg TDS/L. For example, in a recent study using a continuously operated upflow MDC,
more than 99% of NaCl in a salt solution that had a high salt concentration of 30 g TDS/L was removed
at a significant desalination rate of 7.5 g TDS/L/day [
123
]. Ping et al. compared the desalination of
three different types of brackish water at a hydraulic retention time (HRT) of 0.8 day and observed
effective removal of salts and organic compounds [
121
]. As the HRT was increased to 1.7 days,
the MDCs were capable of reducing TDS of brackish water to 110 mg/L, which was close to that of
local tap water (i.e., 90 mg TDS/L) [
121
]. A predictive model for estimating salinity variation and
individual ion concentrations in MDCs was also introduced in the same study for understanding
the key factors in brackish water desalination in MDCs [
121
]. Other researchers investigated the
effects of different low-cost catholyte solutions on MDC performance and observed sound desalination
rates of 9.12 g TDS/L/day and 8.16 g TDS/L/day with bio-catholyte and buffer saline solution,
respectively [
124
]. Moreover, larger-scale MDCs of 105 L were also tested for desalination of synthetic
wastewater containing different concentrations of glucose, and considerable salt removal rate from
3.7 to 9.2 g TDS/L/day was observed [
125
]. Future research may aim to further scale up MDCs for
stand-alone real-world applications with improved yields of freshwater. At the same time, MDCs can
also be integrated with existing membrane-based reverse osmosis facilities to reduce energy demands
during water desalination, which seems more promising in the near future until better system efficiency
and durability of MDCs are upgraded [126].
4.7. Power Supply for Agricultural Monitoring Devices
In recent years, wireless sensor network (WSN) technologies that can automatically collect field
information and perform real-time control of on-farm equipment have been actively developed and
widely applied in agricultural practices to improve efficiency and automation in precision agriculture
activities [
127
]. The agricultural monitoring devices such as remote sensors are typically powered
by batteries or solar energy [
127
]. However, replacing batteries in remote areas is inconvenient and
unsustainable, while using solar systems is inefficient, expensive and highly dependent on weather
conditions [128]. BES technologies such as MSCs and EFCs have been extensively studied to provide
sustainable power supply for WSN devices, with capacitors applied to accumulate excessive energy
generated from these BESs [
7
,
128
–
130
]. Similarly, a specific genre of MFC known as sediment microbial
fuel cell (SMFC) is widely used for powering wireless sensors and small telemetry systems to transmit
the acquired data to remote receivers [
131
]. One of the first SMFCs was developed by Shantaram et al.
over a decade ago by combining an MFC with low-power, high-efficiency electronic circuitry [
132
].
This early SMFC was already able to deliver a maximum voltage output of 2.1 V, which can be
used to power most commercial electronic circuits (required at least 3.3 V) with the aid of a DC-DC
converter to boost the potential [
132
]. For some SMFC applications (e.g., with substrates that are not
Energies 2018,11, 2951 12 of 21
readily biodegradable) that can only generate low potentials and recover electric power interruptedly,
a power management system could be coupled to store and provide stable and continuous power to
sensors [
133
]. The BES technologies can be specifically integrated with different agricultural sensor
systems. Therefore, as the power source, diverse BESs can be used as power diverse wireless sensors
for collecting climatological field data; acquiring irrigation management information; and monitoring
the levels of plant nutrients, pesticides, pH, dissolved oxygen, conductivities, etc. in agricultural
soils [
134
]. Further improvement of the electrode performance and system efficiency will make BESs a
game-changing supplementary for WSN technologies in agriculture.
5. Potential Future Applications of BESs in Agriculture
5.1. Self-Powered Biosensors
BESs can not only power agricultural sensors, but also have the potential to be designed as
self-powered biosensors that can be operated either in situ or online. Comparing with existing
biosensors, depending on anolyte oxidations to provide external voltages, the current generated
by BESs is directly related to the metabolic activities of the electrochemically active biofilm at the
anode [
135
]. Changes of the metabolic activities in response to any disturbances are affecting the
generated current in the circuit. If the operational conditions of BESs are controlled as constants,
the rate change of electron generation can be translated into a signal that represents the magnitude of
any specific disturbance [
135
]. Therefore, in a BES biosensor, the biofilm at the anode is the bioreceptor
for recognizing the specific disturbance, while the transducer is the change of the electric current.
For example, under unsaturated fuel conditions, a change in the organic substrate concentration
(in COD) will lead to a direct change in the generated current, which makes the BES system a biosensor
monitoring the biodegradable organics in the environment; under saturated fuel conditions, the BES
system can be used to detect the level of inhibitors (e.g., toxicants) or stimulators, if all the other
environmental factors are kept constant. In order to be used as biosensors, the BESs must demonstrate
high sensitivity to the target compound near the anode. For BES biosensors, the sensitivity can be
defined as the electric current change per unit anolyte concentration change (normalized by the
surface area of anode) [
135
]. Therefore, with the same change in anolyte concentration, a larger
current change indicates higher sensitivity of the BES biosensor. When applied in real-world systems,
BES biosensors can significantly cut down the maintenance expenses because there are no needs
for external transducers and time-consuming immobilization of bioreceptors. The simplicity of
design and operation also makes BES biosensors more advantageous over traditional chemical and
biological sensors. However, the long-term stability of current output must be further improved for
BES biosensors in order to generate more stable baseline signals [
136
]. Another technical barrier for
BES sensors is to establish the predictive relationships between the signal responses and compound
concentrations of different substrate chemicals [
137
]. To achieve this goal, more accurate mathematical
models should be the tool to help our understanding. In addition, like for other BES applications,
more high-performance but inexpensive materials should be developed for BES biosensors.
5.2. Growing Food Without Sunlight
Traditionally, sunlight is a necessity for plant growth. Plants need light to produce organic
energy molecules such as adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide
phosphate (NADPH) in the chlorophyll. These energy molecules carry high energy and electrons to
the stroma for the fixation of carbon dioxide (CO
2
) into carbohydrates via a reaction cycle known as
Calvin-Benson Cycle [
138
]. In 2016, three researchers (Strik, D., van der Zwart, M. and Buisman, C.) in
Wageningen University proposed the idea to produce food via anaerobic biosynthesis from wastewater
and electricity [
139
]. In this study, energy and electrons generated in BESs would replace the role of
ATP and NADPH produced in the first step of photosynthesis, while nutrients would be recovered from
wastewater to support biomass growth. All can be accomplished in a self-sustaining closed system
Energies 2018,11, 2951 13 of 21
that efficiently utilizes the energy and nutrients recovered via circular pathways. The researchers
named the process dark photosynthesis, which they believe can become practical in the near future
to produce food in areas unsuitable for traditional agriculture [
139
]. Strik et al. estimated that a
dark photosynthesis food reactor of approximately 1 m
3
would be sufficient to provide food for three
people [
139
]. This inspiring research shows the potentials of using BESs for alternative high-quality
and sustainable food production approaches that are more energy- and water-efficient.
5.3. In-Situ Soil Remediation
Agricultural soils are vulnerable to different kinds of contamination, including acidification [
140
],
petroleum hydrocarbon (mainly from on-farm vehicles) [
141
], metals [
142
], and transgenic toxins [
143
],
etc. In order to reuse the contaminated soils for agricultural activities, in-situ remediation is required.
Although BESs have been extensively studied for treating these contaminants in aqueous media,
the effectiveness of BESs in soil remediation has been limited by the inefficient mass transport
(e.g., O
2
and H
+
) in soils [
144
]. However, with appropriate methods to increase soil porosity and
decrease Ohmic resistance, BES-based in-situ soil remediation can be a potent cost-effective tool in the
near future. For example, using a two-chamber soil-MFC inoculated with activated sludge, Zheng et
al. were able to ameliorate acidic soils from pH value of around 5 to nearly 6, while recovering electric
current as high as 123.72 mA/m
2
[
140
]. Another research group succeeded in degrading 82.1–89.7% of
petroleum hydrocarbon (originally 12.25 g/kg dry soil) within 120 days in a pilot study of column-type
BESs that could be directly installed on site for in-situ soil remediation [
141
]. Nowadays, studies on
BES-based soil remediation mainly use MFCs for electric power recovery because MFC technology is
relatively more mature than other emerging BES technologies. However, with future breakthroughs
in ion exchange and mass transport for soil applications of BESs, H
2
energy and other value-added
chemicals can also be recovered on site along with in-situ soil remediation.
5.4. Reuse of Agricultural Wastes in BESs
While BESs can be directly used for different purposes in agriculture to provide economic,
environmental and social benefits, agricultural wastes can also be converted into useful materials
for lowering the high costs of BESs. Many lignocellulosic agricultural residues such as cotton
stalk, rice husk, coconut coir, grass, vegetable fibers can be processed to manufacture construction
materials [
145
], which can be used to build scaled-up BESs for sustainable energy/resource recovery.
In addition, almost all types of agricultural biomass (including animal wastes) could be pyrolyzed
to produce biochar, a novel soil amendment that can significantly improve the nutrient and
water retention in agricultural soils [
4
]. Recent research has also explored biochar’s potential for
contamination treatment [
146
]. The pyrolysis process to produce biochar is often conducted under
oxygen-limiting or oxygen-absent conditions at 300–700
◦
C, and the resulting biochar is usually
characterized with a large specific surface area and good thermal stability [
147
]. Hence, the possibility
to use highly porous electron-conductive biochar materials as the electrodes or electrocatalysts in
BESs has been recently investigated [
148
–
150
]. Huggins et al. [
148
] used biochar electrodes made
from forestry residue and compressed milling residue respectively to construct MFCs and observed
considerable power outputs of 532 and 457 mW/m
2
, which were comparable with those generated
from MFCs using granular activated carbon (674 mW/m2) and graphite granule (566 mW/m2) [148].
According to an economic analysis, the power output cost of biochar electrode MFCs ranged from
$17/W to $35/W, which is significantly lower (over 90%) than those of the MFCs using granular
activated carbon ($402/W) and graphite granule ($392/W) [
148
]. Considering the great potential of
biochar to act as relatively cheaper electrode materials, future studies should focus on investigating
the suitability of more different types of biochar products for BES applications.
Energies 2018,11, 2951 14 of 21
6. Conclusions
Although different aspects of diverse BESs have been extensively studied, agriculture-driven
BES research is limited despite its importance and significance in the face of the challenges relevant
to food security, energy sustainability and freshwater availability. This review has updated recent
agriculture-related BES studies and discussed the current and future BES applications in agricultural
systems. Conclusively, BESs are sustainable technologies that can be integrated into agricultural
systems for energy generation, resource recovery, waste minimization, wastewater treatment, irrigation
water supply, and remote monitoring. It is also possible to design BESs as self-powered biosensors,
as well as for food production and soil remediation. At the same time, agricultural wastes can also be
utilized to construct scaled-up BESs or be pyrolyzed into biochar as lower-cost electrode materials.
Long-term studies should be conducted in the future to assess the system stability and benefits of
on-farm BES applications.
Author Contributions:
S.L. and G.C. conceived and designed the review study; S.L. and A.A. collected and
analyzed the data; S.L. wrote the paper.
Funding:
The research was supported by National Institute of Food and Agriculture, Grant No. 2016-67020-25275;
and National Science Foundation, Grant No. 1735235.
Acknowledgments:
The authors acknowledge the support from the National Institute of Food and Agriculture
through Grant No. 2016-67020-25275 to Florida A&M University and also the National Science Foundation
through Grant No. 1735235 awarded as part of the National Science Foundation Research Traineeship.
Conflicts of Interest: The authors declare no conflict of interest.
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