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Elshobary (2020) Recent Insights Into Microalgae-Assisted Microbial Fuel Cells For Generating Sustainable Bioelectricity

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international journal of hydrogen energy xxx (xxxx) xxx

Available online at www.sciencedirect.com

ScienceDirect

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

Recent insights into microalgae-assisted microbial


fuel cells for generating sustainable bioelectricity

Mostafa E. Elshobary a,b,1, Hossain M. Zabed a,1, Junhua Yun a,


Guoyan Zhang a, Xianghui Qi a,*
a
School of Food & Biological Engineering, Jiangsu University, Zhenjiang, 212013, Jiangsu, China
b
Department of Botany and Microbiology, Faculty of Science, Tanta University, Tanta, 31527, Egypt

highlights graphical abstract

 Algae-assisted microbial fuel cell


(MA-MFC) can generate sustain-
able bioelectricity.
 Configurations MA-MFC and its
bioelectricity generation are criti-
cally reviewed.
 Bioelectricity production in MA-
MFCs is a tricky multi-parameter
microbial process.
 Progressive optimization needed
to maximize the benefits of MA-
MFCs.
 Application, challenges and pros-
pects of MA-MFC are highlighted.

article info abstract

Article history: Power generation from the renewable biomass sources using microbial fuel cell (MFC) has
Received 27 December 2019 attracted significant attention in recent years, while chemical energy stored in microalgae
Received in revised form biomass has efficiently been used for the sustainable production of biofuels and other
12 June 2020 valuable bioproducts since the decades. The usage of these photosynthetic organisms in
Accepted 25 June 2020 MFC can enhance the efficiency of MFC and provide a cost-effective and renewable
Available online xxx approach for the bio-generation of electricity. Microalgae are commonly incorporated
either with anode or cathode compartment of MFC to generate electron or oxygen,
Keywords: respectively. Despite microalgae-assisted MFC (MA-MFC) would be more sustainable than
Algal biomass using MFC alone, further developments in such systems are still required for improving its
Microalgae-assisted MFC efficiency and achieving a real-world application on a large scale. In this context, under-
Bioelectricity standing in bio-electrochemical mechanism of MA-MFC, including electrons shuttle and

Abbreviations: BES, bioelectrochemical systems; COD, chemical oxygen demand; DO, Dissolved oxygen; Pmax, maximum power; MA-
MDC, Microalgae Assisted Microbial Desalination Cell; MFC, microbial fuel cell; MA-MFC, microalgae-assisted microbial fuel cell; OCV,
open-circuit voltage; OLR, organic load rate.
* Corresponding author. School of Food and Biological Engineering, Jiangsu University, 301 Xuefu Road, Zhenjiang, 212013, Jiangsu,
China.
E-mail address: qxh@ujs.edu.cn (X. Qi).
1
M.E. Elshobary and H.M. Zabed contributed equally to this work.
https://doi.org/10.1016/j.ijhydene.2020.06.251
0360-3199/© 2020 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
2 international journal of hydrogen energy xxx (xxxx) xxx

Biofuel oxygen generation, is very important. Moreover, many factors can limit the efficiency and
Fuel cell performances of MA-MFCs that are needed to optimize in further research efforts. This
Photosynthesis review presents a comprehensive insight into MA-MFC, including the recent developments
and potential challenges in this promising bio-electricity generating system. Specifically, it
focuses a critical discussion on the configurations of MA-MFC, key operating parameters
affecting performances of MA-MFC, challenges and prospective research works for
improving the overall energy output of MA-MFC.
© 2020 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

much as 9% conversion efficiency [23]. Moreover, algae have


Introduction some advantages over higher plants, including high growth
rate, availability in all seasons, capable of cultivating in the
Rapid exhaustion of fossil fuel resources and growing concern non-arable lands, and non-competitiveness with food and
with global warming resulting from the increased usage of the feed crops, which have their potential biomass feedstocks
conventional fuels are the distasteful problems across the [4,24,25]. Typically, the photosynthesis process is begun with
world that is threatening the survivability of the entire hu- the light photon induction and ended with carbon fixation in
manity [1e3,236]. Growing industrialization with increased different forms such as carbohydrates, lipids, proteins, etc.,
populations has led to an increase in fossil fuel consumption, and oxygen as one of the byproducts.
which resulted in increasing CO2 emissions, as well as global Therefore, utilizing algal biomass or even living algae
warming, which consequence many disasters such as floods, directly for energy generators can be a promising approach.
hurricanes, forest fires, and damage to the ecosystem [4,5]. Recent advances in the MFCs have added an enormous scope
Emissions of CO2 due to the consumption of fossil fuels has for bioelectricity generation via microbial metabolism. Mi-
been estimated to increase from 388.5 ppm in 2009 to crobial fuel cells are devices that depend on a biocatalytic
409.95 ppm by 2019, within only ten years [6]. On the other reaction carried out by the electroactive microorganisms
hand, current energy provisions and electricity generations (such as bacteria or yeast) to generate clean bioelectricity [26].
are solely dependent on fossil fuels [7,8]. To ensure energy Despite, bacteria are the most commonly used microbes in
security and reduce CO2 emissions, it is of utmost importance MFCs, many of them are not efficient to generate electrical
to develop alternative clean energy sources. Clean energy current [27] and they may need a high feeding rate and
technologies, namely, solar, wind, hydro, biomass, effective electron acceptor to increase energy output, but it is
geothermal, tidal, and wave power technologies, are not cost-effective to use [23]. Thus, bacteria-assisted MFCs
improving very rapidly. These renewable energy sources are can be replaced with most oxygen generator bioactive
superior to fossil fuels for offering several environmental microalgae. While the photosynthetic process can provide
benefits, while the main problem with these renewable re- electrons flow for the current generation at the anode side
sources is the difficulty to store or transport energy produced and O2 as a sustainable electron acceptor at the cathode side
[9e11]. of the MFCs. Electrochemical microalgae were reported to
Recently, electrochemical energy storage devices have show promising results compared to bacteria in terms of
received much attention from the scientific and industrial electricity generation and energy consumption [28]. The
societies because of its excellent superior power density, rapid continuous power output of 539 mA m2 for five months was
charge/discharge rate, and long lifecycle such as super- performed by developing microalgae-assisted MFCs (MA-
capacitors and micro-supercapacitors [12e14], two- MFCs) coupled to photobioreactor [29]. Further, MA-MFCs
dimensional materials [15] and bioelectricity devices [16,17]. could be integrated with a variety of promising applications
As a promising sustainable approach, especially with regards such as bioremediation, biomass and biodiesel production as
to the feasibility of wastewater treatment and CO2 seques- well as CO2 migration. Different configurations of MA-MFCs
tration efficiently [18], bioelectricity devices can directly with a diverse electrode [30,31], a variety of substrates, and
generate electricity from degradable organic matter using microbes have been employed [32,33] to maximize the ben-
different biological processes. efits of MA-MFCs.
Recently, utilization of the photosynthesis process as a The main objective of this review is to present an insight
source for renewable energy by generating hydrogen,
into the generation of bioelectricity through MA-MFC. In this
bioelectricity and other biofuels, have been considered effi-
cient alternatives to fossil fuels [19e21]. Photosynthesis pro- context, relevant perspectives are critically discussed
cess depends on the conversion of solar energy into chemical focusing on the overviews of MFC an MA-MFC, principles of
energy for biomass production, whereas conversion efficiency MA-MFC, configurations of MA-MFC, power generation of MA-
varies according to the species of photosynthetic organisms.
MFCs, factors affecting MA-MFCs, MA-MFCs applications,
The conversion efficiency can range from 4.6% to 6% in higher
limitations in MA-MFC, and challenges in improving energy
plants [22], while algae represent the highest conversion effi-
ciency among the photosynthetic organisms providing as output.

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
international journal of hydrogen energy xxx (xxxx) xxx 3

compounds to the anode without using a mediator. The power


Microbial fuel cells (MFCs) and microalgae- maximum in MFC is still a hundred times smaller. This
assisted MFCs (MA-MFCs) reduction in power generation and thermodynamic limitation
has led to the invention of different configurations and im-
MFCs can convert chemical energy stored in the organic provements in MFC. So far studied, algae and MFC integration
matter of biomass into electrical power. Each MFC usually been found promising with respect to efficiency as Yagishita
consists of an anode (negative pole), a cathode (positive pole), et al. [49] established a system that converted light energy into
and electrolyte(s). Ion exchange membrane (IEM) may be electrical power with a conversion efficiency of only 3%. Re-
located between the cathodic and anodic compartments searches on the microalgae-assisted MFCs have been exten-
(Fig. 1). The anodic chamber has microorganisms in a liquid or sively established [50,51], with their integration leading to the
attached as a biofilm that oxidize organic substrates and development of microalgae assisted-MFC (MA-MFC) [52]. With
generate electrons, protons, and other metabolites as the end the research progresses in MFC, the number of publications on
products. The basic MFCs utilize a variety of organic sub- MFC has also been increased significantly over the last 20
strates, including sugars [34e36,238], acetate [37], alcohols years (Fig. 2). As per the records in the Web of Science (WoS)
[38,237], organic compounds [35,39] or even wastewaters [40]. database searched by using the topic of ‘‘microbial fuel cell”,
Electrons produced in the oxidation reactions flow through an total publications on MFC increased from 13 in 2000 to 1197 in
external circuit, which results in a current flow from the 2018, which followed a small decrease in 2019 (Fig. 2).
cathode to the anode, while protons transfer through a sepa- MFC is an innovative tool that has been marked for its high
rator, such as a proton exchange membrane into the cathodic efficiency under the mild condition without requiring any
chamber to react with the electrons, thereby reducing oxygen external energy source, and can work with low-cost sub-
into water [41]. strates [53,54]. Major limitations of MFC are environmental
The concept of using microorganisms to generate elec- toxicity, cost of electrode materials, and availability of the
tricity was first observed at the beginning of the 20th century final electron acceptor at the cathode part. These obstacles
by Potter [42] using Escherichia coli as the electrogenerator, but could be overcome by using bio-electrolytes, especially if the
the cell generated a small current of 0.2 mA. In 1931, Cohen biocathode chamber had an oxygenator organism to reduce
[43] designed microbial half fuel cells in series to increase the the costs and work as a final electron acceptor [28]. The only
voltage to around 35 V with 2 mA current. Later, Sisler [44,45]; microorganisms that can generate O2 normally on this planet
Davis and Yarbrough [46], and Davis [47] have used different at a faster rate than any other type of plant are microalgae that
microorganisms to generate electricity. In the early 1990s, the include eukaryotic algae and prokaryotic cyanobacteria [31].
fuel cells became more appealing devices after the principle of One of the most talented advances in MFCs is the utiliza-
MFC was discussed by Allen and Bennetto [48]. A series of tion of solar energy by the photosynthetic microalgae for
progress followed in later years, increasing the power density bioelectricity production, and many studies have been re-
of this device and reducing its constituent and operational ported on MA-MFCs in recent years [23,55e58]. Microalgae are
costs [43e45]. In this period, MFC depended only on bacteria renowned photosynthetic organisms [59,60], which have po-
which can directly transport electrons via oxidation of organic tential to produce bioelectricity by incorporating with MFCs.

Fig. 1 e Schematic diagram of a typical microbial fuel cell with anode chamber and cathode chamber sandwiched with a
proton exchange membrane (PEM).

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
4 international journal of hydrogen energy xxx (xxxx) xxx

Fig. 2 e Number of publications on the MFC in the Web of Science (WoS) under the keyword “Microbial fuel cells” until June
6, 2020.

The MA-MFCs depend on the autotrophic microalgae that can Photosynthesis mechanism
convert solar energy into electricity through the photosyn-
thesis process. Living microalgae can be used as an electron Microalgae convert solar energy into different forms of
generator at the anode or electron acceptor at the cathode chemical energy using CO2 directly from the atmosphere.
using oxygen derived from microalgal photosynthesis [28,31]. Sun-light is captured via the chlorophyll’s antenna and
In the ex-situ MA-MFC systems, a separate photobioreactor is transferred to the special chlorophyll dimer (P680 of photo-
required to get the highest algal growth for optimal electricity system I and P700 of photosystem II). Once photon excited
generation [23]. On the other hand, microalgal biomass can these chlorophyll dimers, electron transportation initiated
also be used as a substrate for microbial oxidation at the through various transporter (Plastoquinone (PQ), Cytochrome
anode part. In addition to bioelectricity generation, MA-MFCs b6F (Cyt b6F), Plactocyanine (PC)) and across membranes to
can also capture atmospheric CO2 and remove contaminants produce ATP [64]. Ferredoxin enzyme receives electrons from
from the wastewaters [61,62]. PSI and transfers them to ferredoxin NADP þ oxidoreductase
(FNR) to generate NADPH that can be utilized in dark reaction
for CO2 fixation (Fig. 3). Deviation from the normal electrical
Principles of MA-MFCs conditions can split two water molecules into four photons to
yield one oxygen molecule, four exciting electrons and four
Principles of MA-MFCs include four basic steps, which are protons as shown in Eq. (1) [65], where two photons are uti-
photosynthesis, transport of electron to the anode, anodic lized to reduce each molecule of NADPþ (Eq. (2)).
oxidation of organic matter by the electrochemically active
bacteria and cathodic reduction of oxygen. The conversion of 2H2 O þ 4hv/O2 þ 4Hþ þ 4e (1)
solar energy into bioenergy by MA-MFC is a significant prog-
ress in the generation of renewable electricity. Microalgae 4hv þ 4e þ NADP þ 4Hþ /2NADPH þ 2Hþ (2)
have been used in the MFC in the cathode to provide oxygen or
Electron transfer mechanisms
anodes as electron donor-substrate for bacterial growth. In
addition, bioelectricity generation does not depend solely on
Transfer of electrons from microorganisms to the anode in
light time, but it has observed an increase in power generation
MFC can be accomplished by several mechanisms. The main
during the dark phase [63]. The MA-MFC system is similar to
concept is based on the transfer of electrons from anode to the
MFCs in the necessity of the presence of an anode and cathode
cathode through an electric circuit, whereas protons diffuse
assembly for carrying out oxidation and reduction reactions,
through the membrane to reduce oxygen at the cathode. The
respectively. The overall activity of MFCs depends on the
electron transportation is an extracellular process either in
redox reactions [28]. In the anodic side, the oxidation process
microalgae or bacteria, where electrons are usually trans-
occurs via microbial degradation or photosynthesis process
ferred from the substrates and to the anode directly via cyto-
and electron transferred to the anode electrode directly or
chromes located in the cell membranes [66,67].
indirectly. On the other hand, the reduction reaction per-
Some cyanobacteria species have organelles that can
formed in the cathode-side by using photo-generating oxygen
transfer electrons to an external anode, called pili, which are
as an electron acceptor.

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
international journal of hydrogen energy xxx (xxxx) xxx 5

Fig. 3 e Schematic representation of photosynthesis pathway eukaryotic microalgae.

cellular projections on the cell membrane. Pili mainly control reaction can be classified into either aerobic or anaerobic re-
cell to cell communication and phototaxis in cyanobacteria actions depending on the source or nature of the final electron
[68]. Pili also can be used as electrically conductive filaments acceptor. In anaerobic cathode, different pollutants such as
[41]. In MFCs, pili can act as spacers or ‘nanowires’ to transfer NO3 (nitrification), SO4 (sulfate reduction), or CO2 (methano-
electrons between cells to anode surface [69]. genesis) can act as a terminal electron acceptor (TEA), while O2
Electron shuttling is another possible mechanism of elec- is the TEA in the aerobic condition [74,75]. In addition, the
tron transfer, which involves cyclic diffusion of the soluble origin of oxygen is differed according to the configuration of
substrate as a mediator into a microbe in oxidized form after fuel cells. It can be atmospheric O2 in the air cathode of the
oxidizing at the anode. Generally, in this mechanism, a fuel cell. Some other configurations are used in the mechan-
mediator is used in the cathode compartment for electrons ical aeration. However, while using oxygenator, photosyn-
shuttling. Electrons are transferred from the anode into the thetic microalgae were reported to show challenging results
cathode to reduce the oxidized mediator, which then enters compared to those of other sources in terms of both economic
into the microalgal cells to further oxidize and then release and environmental aspects [28]. The O2 level in the cathodic
their electrons. Microalgal cells release oxidized mediator to chamber determines the performances of cathode. O2 is an
the media, and the cycle is thus repeated [70,71]. These elec- ideal TEA for its nontoxic effect and renewability, high stan-
tron mediators can be added externally [48] or naturally pro- dard redox potential (0.82 V), inexhaustibility, and readily
duced by microalgae themselves [72]. This proved that availability [76]. Microalgae serve as the renewable source of
microalgae could be used as electron donors in the anodic side oxygen via photosynthesis process that can increase the level
in MFCs for generating electricity. of O2 in the cathode side to increase MFC cathode potentials
and power densities [77] and to decrease cathode over-
Oxidation of organic matters at the anodic compartment potentials as most of the active cathodic sites are involved in
reaction [78,79].
In this process, different biodegradable microorganisms,
mostly bacteria, are used to degrade externally driven organic
matters or produced by microalgae. However, this oxidation Configurations of MA-MFCs
process depends on the liberation of electrons from the mi-
crobial cell to the anode, unlike other biochemical and cellular In general, the configuration of MA-MFC can be four types,
processes, where electrons are transferred through a redox which are single chamber, double chambers, dual chambers,
reaction. But unfortunately, not all biodegradable microbes and algal sediment. Single chamber configuration was
are electrochemically active; and even most of them are designed by several researchers [80e82]. This is the simplest
inactive [27]. The most common electrochemically biode- design that permits microalgae to generate electrical power
gradable microbes are Shewanella sp.,.Geobacter sp.,.Rhodoferax using only one chamber.
ferrireducens,.Rhodopseudomonas palustris, Ochrobactrum
anthropi, Desulfovibrio desulfuricans, D. acetoxidans, Acidiphilium Single chamber
sp. Thermincola sp. and Cupriavidus basilensis [73]. Mixed bac-
terial culture usually generates a higher oxidation rate and Single chamber MFCs are classified into two subtypes ac-
power densities in MFCs than the axenic bacterial strains [31]. cording to the nature of the cathodic medium, wet cathodic-
and air cathodic single chambers as illustrated in Fig. 4. In the
Cathodic reduction of oxygen wet cathodic configuration, microalgae perform photosyn-
thesis under light and produce electrons and protons
The reduction of oxygen is the final critical step of the elec- depending on the utilization of CO2 and light (Eq. (3)). In this
trochemical process in MA-MFCs. The cathodic reduction process, organic substances, algal biomass, and oxygen are

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
6 international journal of hydrogen energy xxx (xxxx) xxx

Fig. 4 e Schematic configuration of single-chamber algal-MFC; (A) microalgae catalyzed design wetted cathode (B)
microalgae coculture bacteria catalyzed design air cathode.

produced as the final products. The released oxygen during be added to the anodic chamber to allow electrons to shuttle
photosynthesis is consumed by microalgae in the dark respi- from the fermentative cells to anode (Fig. 5).
ration process to degrade the organic matters and further
production of electrons and protons during the dark period Dual chamber
(Eq. (4)).
The dual-chamber MA-MFC is known as the most common
Lights
6CO2 þ 12Hþ ƒƒ!C6 H12 O6 þ Biomass þ 3O2 (3) configuration made by using microalgae as oxygen generators
in the cathodic side of MFC [84e86]. This configuration is
Oxidation consisting of two chambers separated by a proton exchange
C6 H12 O6 þ 6H2 Oƒƒƒƒ!6CO2 þ 24Hþ þ 24e (4)
membrane (PEM). Generally, wastewater treatment is inte-
In the wet cathodic fuel cell, cathode and anode were grated with this type of MFC, where activated sludge is used in
soaked in the same fluid of fuel cell where protons travel to the dark anodic compartment and microalgae culture in the
the wet cathode without any mediator or ion-exchange light cathodic side [87]. CO2 produced by the anodic bacteria is
membrane to be oxidized inside the fuel cell (Fig. 4A). Air transferred to the cathode compartment to be utilized by
cathodic single-chamber MFCs differ from the previous one by microalgae (Fig. 6).
the usage of the ion-exchange membrane for transporting
protons to the cathode that is located outside the fuel cell
exposed to the air to use atmospheric oxygen as a final Sediment MFC
acceptor. Pure algal culture can be used in this design or mixed
with some degradable bacteria to enhance electron generation The generation of bioelectricity in the sediment MA-MFCs
and performance of MFC using organic materials produced by depends on the natural differences in electro-potential [88]
microalgae as a substrate for bacterial degradation (Fig. 4B) created using a sediment buried-anode and immersed-
[83]. cathode on top of the sediment. Electron flow is achieved
through the decomposition of organic or inorganic com-
Double chamber pounds in sediments by microorganisms, while generated CO2
is consumed by microalgal cells in the upper cathodic
In the double chamber MA-MFC, two separated compartments compartment, and O2 produced by microalgae acts as the final
are maintained in the absence of ion-exchange membrane, electron acceptor [89] (Fig. 7). Recently, Wang et al. [61] have
where algal cells are cultivated in one chamber under light constructed a sediment MA-MFC using C. vulgaris based-
condition and fermentative microorganisms are grown in the cathode. Usage of microalgae in cathode improved its per-
other chamber in dark condition. This setup depends on the formance by generating a suitable amount of the O2 in situ that
degradation of the organic matters (e.g. wastewaters) by works as the final electron acceptor. The maximum power
fermentative microorganisms to produce electrons that move output was of this MA-MFC was 21 mW m2, which was
via external circuits plus CO2 utilized by the photosynthetic further increased by 2.4-folds after adding carbon nanotube
microalgae to reduce electron at the cathodic chamber. This coated cathode. On the other hand, microalgae can be used in
configuration operates in the absence of an ion-exchange the anode side of the sediment MA-MFCs to discover electro-
membrane, which simplifies its structure and makes it cost- genic microalgae and cyanobacteria [91]. For example, poly-
effective for scaling up. However, a chemical mediator must styrene anodic benthic side can be filled with benthic soil

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
international journal of hydrogen energy xxx (xxxx) xxx 7

Fig. 5 e Schematic configuration of coupled algal-MFC.

Fig. 6 e Schematic configuration of dual chambers algal-MFC.

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
8 international journal of hydrogen energy xxx (xxxx) xxx

Fig. 7 e Schematic configuration of algal sediment MFC (algal-SMFC).

samples from marine or other environments under the light Microalgae based-anode
irradiation. Different electrogenic microalgae and cyanobac-
teria are attached to the anode, such as Pseudanabaena, In this configuration, electrogenic microalgae are used in the
Leptolyngbya, Chroocococales, Phormidesmis, Microcoleus, anode as electron donors to generate bioelectricity either
Nostoc and Phormidium. Paulschulzia pseudovolvox as a through the photosynthesis process in autotrophic algae or
benthic strain of Chlorophyceae showed the maximum power degradation of organic compounds in heterotrophic algae.
density compare to the other strains [91]. Nevertheless, generating oxygen by algae in the anodic part
causes a serious problem for the MA-MFC as oxygen is an
electron acceptor that might reduce the electron flow signifi-
Power generation by the algal MFC cantly. However, microalgae-based anode depends on the
utilization of the generated O2 by the same microalgae in the
Usually, microalgae could be cultivated in the anodic or dark reaction or by other cocultured bacteria in the oxidation
cathodic chamber of the algal MFC. Anodic microalgae are of the organic substrate. Markedly, most of the anodic
generated current directly as a result of the assimilation of microalgae configurations are restricted in single-chambered
organic or inorganic substrate producing electrons that fuel cell design. In one previous study, C. pyrenoidosa was
transferred to the anode. However, cathodic microalgae used introduced in the anode of air cathodic MFC [92], which re-
as bio-oxygenators to accept the electrons. Several workers ported maximum power density 6.03 W m2anodic more than
were configurated different algal MFCs to obtain the facilitate 200-folds than that obtained from bacterial MFC (0.03 W m2).
the operation and enhance the energy output of the algal In another work, living cyanobacteria, particularly Spir-
MFCs either an anode or cathode sides [23,30]. ulina platensis, were attached to the anode of the MA-MFC

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
international journal of hydrogen energy xxx (xxxx) xxx 9

chamber without a membrane and using cultivation medium C. vulgaris also could be used as biocathode in the double-
as a mediator to generate bioelectricity via the consumption of chambered- MFCs by cultivating C. vulgaris in a tubular pho-
intra-biochemical compounds produced during photosyn- tobioreactor as a bio-cathodic chamber. Maximum power
thesis. The highest electrical power (1.64 mW m2) was output reached 21.4 mW m2 higher than that obtained by an
recorded in the dark with the highest voltage (390 mV) abiotic cathode by more than 2.5-fold. C. vulgaris were also
comparing to the day time electrical power that did not exceed used as a suspended or immobilized form in the cathodic
0.132 mW m2 [93]. Lin et al. (2013), have used the same design chamber of MFC [100]. The immobilized form showed the
of MA-MFC but by using S. platensis biofilm on the anodic greatest energy production (2.5 W m3) higher than that ach-
electrolyte. Results showed that the maximal open-circuit ieved by the suspended form. This method also achieved an
voltage (OCV) of MA-MFC (490 mV) and the maximum power 84.8% COD reduction with zero discharge of CO2 in a process
density reached to 10 mW m2 when connected to an external called microbial carbon capture cell (MCC) [71]. Zhang et al.
resistance of 1 kU. [29] studied microalgae (Chlorella sp. QB-102) as a biocathode
Mixed microalgal culture in the anode compartment was in MFC for power generation and Cdþþ removal using nickel
also used in the membrane-design MA-MFC [94]. But very low foam/graphene (NF/rGO) as electrodes. It was found that the
power density was achieved (4 mW m2) due to the different maximum power density obtained by using NF/rGO was
strains in the mixed culture have different abilities toward 36.4 mW m2. This algal MFC further improves the removal of
generating electron flow rate to the anode. Also, low power Cd(II) of almost 95% with a maximum adsorption value of
output might be attributed to the nutritional mode that was 115 g m2. Zhou et al. [101] studied the performance of double
used during the experiment setup. Generally, using oxygenic chamber MFC using Scenedismus obliquus as a biocathode. The
microorganisms at the anode shows low-performance MFC O2 produced by these photosynthetic algae exhibits the
due to the high redox generated by oxygen evolution at the maximum power density (153 mW m2 cathode) comparing to
anode, in contrast, using oxygenic species at the cathode the mechanical aeration (116 mWm2) and a voltage genera-
showed more impressive results [62]. tion of 470 mV was achieved using 1000 U external resistance.
Recently, MFC was integrated with algal biofilm to maxi-
Microalgae-based cathode mize the system’s benefits for nutrient removal and bioenergy
production; this fuel cell called algae biofilm microbial fuel cell
One of the main constraints to the practical implementation (ABMFC) using microalgae Scenedesmus quadricauda [62]. The
of MFC is the finding of effective and sustainable cathode maximum power density of the ABMFC reached to
semi-reaction catalysts to avoid costly and/or toxic catalysts. 62.93 mW m2 was higher than that of the MFC
It also needs high energy to sustain an optimal level of dis- (52.33 mW m2) by18%. This setup showed significant removal
solved oxygen [95]. Using phototrophic organisms is one of the of TN, TP and COD of 96.0%, 91.5% and 80.2%, respectively,
advantageous options because it can be used as an effective higher than MFC or AB alone. Da Costa and Hadiyanto [102]
in-situ oxygen generator and its ability to capture CO2. Plat- investigated dual-chamber algal MFC using watermur as a
inum is one of the most effective catalysts commonly used in proton exchange membrane for bioelectricity production and
MFC, but it is expensive to expand MFC systems for large-scale wastewater treatment. Cyanobacteria Spirulina platensis was
applications. On the other hand, ferricyanide is also usually cultivated at the cathodic chamber and tapioca wastewater as
used in laboratory-scale MFC systems, while not as costly but an anodic compartment. The plateau power density was
needs to be replenished and is toxic to the environment [96]. 44.33 mWm2 with maximum current-voltage (0.166 V) on the
Microalgae-based biocathodes depend on the photosyn- 6th day.
thesis process that allows phototrophic microalgae to use CO2
as a carbon source and generate O2 [96e98]. Algal biocathode Algae as feedstock for MFC
helps in the wastewater remediation through anodic oxida-
tion and cathodic reduction simultaneously with sequestra- Most recently, algae have been investigated not only as an
tion of CO2 at the cathodic compartment to produce biomass oxygenator at the cathode compartment or electron donor at
[31]. As microalgal bio-anode, biocathode can be configurated the anode side but as a possible fuel for MFC. It is known that
in an air-exposed single-chamber fuel cell or double chamber. many bacteria and yeast species can degrade biomass,
Chlorella is one of the most popular microalgae used as including microalgae at the anodic MFCs [103], Microalgae
biocathode (Table 1). C. vulgaris was immobilized on the biomass mainly consists of proteins, carbohydrates, and lipids
cathode electrode and exposed to air for bioelectricity gener- [104]. All these components considered as a high energetic
ation and wastewater bioremediation using dye textile compound that can release enough electrons for bioelectricity
wastewater. The maximum power density generated was generation in MFCs. It has been demonstrated earlier that
123.2 mW m3 [99]. This method was able to biotreatment of algal biomass (obtained by centrifugation, filtration, dried,
dye textile wastewater and effective removal rates of chemi- ground into a fine powder, and/or treated by different pro-
cal oxygen demand (COD) (92e98%) and heavy metals cesses) are appropriate for bioelectricity production [76].
(54e98%). Marine Chlorella sp. also used in single MFC but by Interestingly, algal biomass can be fed in a cathodic or anodic
mixing with wastewater in a membrane, buffer and catalyst- compartment.
free MFC. The results showed the maximum power output Two different algae have been used as a feedstock dried
of 4.06 mW m2, current density of 46.34 mA m2 with open powder at the anodic single-chamber MFCs namely C. vulgaris
circuit potential of 0.43 V and low internal resistance of 611.8 U (microalgae) and Ulva lactuca (macroalgae). C. vulgaris feed-
[57]. stock generated power density (980 mW m2) higher than that

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Table 1 e Maximum power (Pmax) production using microalgae at anode, cathode or as substrate for power generation.
Group Species Function Type of MFC Pmax Pmax Ref.
(mw m2) (mw m3)
Cyanobacteria Spirulina platensis Bioanode Single chamber e 1.64 [93]
S. platensis Bioanode Single chamber 10 e [80]
Synechocystis sp. Bioanode Two-chambered e 6.7 [69]
Mixed Cyanobacteria Bioanode Two-chambered 72 e [184]
Microalgae Mixed microalgae Bioanode Single chamber 76 1060 [209]
Mixed microalgae Bioanode Single chamber 0.003 0.005 [94]
Chlorella pyrenoidosa Bioanode Dual chamber 30.2 120a [92]

Cyanobacteria Microcystis aeruginasa Biocathode Dual-chamber e 58 [210]


Microalgae C. vulgaris Biocathode Dual-chamber 13.5 e [142]
C. vulgaris Biocathode Dual-chamber 18.7 e [211]
C. vulgaris Biocathode Dual-chamber e 2485.35 [71]
C. pyrenoidosa Biocathode Dual-chamber 2.5 450a [92]
Desmodesmus sp. Biocathode Dual-chamber 64.2 820 [112]
Scenedesmus acutus Biocathode Dual-chamber e 400 [133]
Mixed microalgae Biocathode Dual-chamber e 2800 [212]

Cyanobacteria Cyanobacterial blooms Biocathode sediment 16.7 e [213]


Microalgae Mixed microalgae yanobacteria Biocathode sediment 11 e [214]
C. vulgaris Biocathode sediment 68 e [138]
C. vulgaris Biocathode sediment 38 e [90]
C. vulgaris Biocathode sediment 48.5 e [32]
Mixed microalgae Biocathode sediment 22.19 e [137]
Mixed microalgae Biocathode Dual-chamber e 5700 [212]

Cyanobacteria Microcystis aertiginosa Substrate Two-chambered e 4140 [215]


Arthrospira maxima Substrate Two-chambered e 100 [216]
Synechococcus leopoliensis Substrate Stack of 9MFCS e 4250 [105]
Cyanobacteria Substrate Single chamber 114 2570 [217]
Microalgae C. vulgaris Substrate Single chamber 980 2770 [23]
C. vulgaris Substrate Two-chambered e 3700 [215]
C. vulgaris Substrate Two-chambered 15 370a [126]
Dunaliella tertiolecta Substrate Two-chambered 5.3 672a [126]
Scenedesmus obliquus Substrate Two-chambered 102 950a [218]
Scenedesmus sp. Substrate Two-chambered 1780 e [219]
Mixed algae Substrate Two-chambered 207 1035 [220]
Mixed algae Substrate Two-chambered 110 e [221]
Macroalgae Larminaria saccharina Substrate Two-chambered 218 e [222]
Ulva lactuca Substrate Single chamber 760 2150 [23]
a
Calculations are based on the given information.

produced by U. lactuca (760 mW m2) with energy generation Most recently, algal biomass suspensions were subjected
of 2.5 kWh kg1 while U. lactuca showed a high degradable rate to three thermal pretreatment conditions at 25, 55 and 95  C,
superior to C. vulgaris [103]. Untreated fresh algal biomass has for 24 h before used in MFCs to test the bioenergy production
also been used in MFCs directly without centrifugation, dry- and MFCs performance. The results showed the best pre-
ing, grounding and/or treated by acid-thermal processes. In treatment temperature was 25  C with maximum energy
this technique, an adapted pre-digester Synechococcus leo- production (57.06 mWm2) and 220 mV of current-voltage
pliensis was used to generate light-driven electricity using 9 [108].
cascade fuel cells to achieved 42 W power continuously for On the other hand, the whole MFCs can be performed by
2e4 days [105]. microalgae in both electrolytic chambers by using algal
Khalfbadam et al. [77] innovated a new technique to supply biomass in the bio-anode chamber and living microalgae in
fresh algal biomass directly from photobioreactor to the the cathodic side. This MFC depends on the utilization of
anionic chamber of MFC without further costly pretreatment CO2 that released in the anodic chamber to grow living
process. This technique called bioelectrochemical systems microalgae in the cathodic chamber. In this context, dead
(BES), which has been used for the first time to entrap, microalgae biomass of Scenedesmus sp. (collected from
decompose and oxidize fresh algal biomass from algal pho- polluted streams) was as a substrate at the anodic side and
tobioreactor to generate a stable current of 6.2 mA for over 70 living C. vulgaris was used in the cathodic chamber of MA-
days. Moreover, BES can remediate wastewater by removing MFC. The highest power density of 1900 mW m2 with a
soluble organic matter and chemical oxygen demand and Coulombic efficiency of 6.3% was obtained at 2.5 g COD L1
suspended solids [107]. of microalgae biomass (0.5 g L1) [33]. Another study used a

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double-chamber MA-MFC fed with the decomposed cyano- that can affect electricity generation by affecting the
bacteria mixture at both the anodic and the cathodic photosynthesis process. Lan et al. [82] studied the impact of
chambers for power generation and the nitrogen removal monochromatic red, and blue light of 620e750 nm and
[109]. The results showed that a maximal power recovery 450e495 nm, respectively on Chlamydomonas reinhardtii
was 1.28 mW m2 coupled with 64 g TN m3 day1 nitrogen assisted anode and reported that red LED light enhanced
removal. In a recent study, C. vulgaris was cultivated in the power density to 12.95 mW m2, which was more than 60%
cathode chamber and its extracted lipid was used as an higher than to the power density provided by the blue LED
electron donor substrate in the anodic chamber [110]. The light at the same intensity (900 lx). This phenomenon might
performance of MA-MFCs fed with extracted lipids was be due to the increase in growth rate when cultivated in
superior to that feed with fruit waste in all aspects. the wavelength of red light ranging between 650 and
Maximum 2.7 W m3 power density was obtained by the 750 nm (Fig. 8). It had led to enhance photosynthesis pro-
extracted lipid-fed MFCs, which was 1.45 and 2.60 folds cess and electron flow rate, as well as the power output.
higher than those provided by the fruits waste-fed MFC and Moreover, the results of the above study showed that total
control MFC (pre-treated cow manure) respectively. The chlorophyll content increased with the increase in light
system was able to generate an electric energy 136 Wh Kg1 intensities and a better performance of MA-MFC can be
COD day1, 782 Wh m3 day1 of algal oil energy and achieved at a relatively higher light intensity.
28 g m3 day1 of algal productivity. On the other hand, excessive light intensity can affect
algae-based cathodes by affecting O2 evolution rate on the
Factors affecting MA-MFC photosynthesis process. Wu et al. [83] studied the effects of
different light intensities (0, 1500, 2000, 2500, 3000, 3500 lx)
Source and intensity of the light on MA-MFC using Desmodesmus sp. A8 in the cathode. It
was reported that anode and cathode resistances as well as
The source of light and light intensity are critical factors in the generation of bioelectricity were significantly affected
MA-MFCs using algae either in an anode or cathode side by the light intensity. They also investigated that dissolved
oxygen (DO) in the cathode biofilm increased by an increase
in the light intensity, as it is an indicator for boosting
photosynthetic rate.

pH value

Neutral pH (6e8) is the optimal pH for an excellent perfor-


mance of MFC and metabolic activity of microbes in both
anode or cathode chambers [23,113]. However, proton pro-
duction during photosynthesis in MFCs leads to acidification
of the anode compartment [114]. Accumulation of protons
creates a pH gradient resistance, which causes a loose of pH
gradient potential over time [29], which can reduce current
density and electrode potential [114,115].
Under the optimum conditions, cathode reactions reduce
O2 by protons and electrons to produce water. Any imbal-
ance in the electrons, protons, or O2 level leads to a change
in pH gradient and decreases electricity production. The
ideal cathode potential is 0.81 V at pH 7.0, but in practice,
experimental value is always lower than this standard value
due to the mixed potential of contaminating species.
Moreover, on non-noble (oxidizable and corrodible) metal
catalysts such as carbon electrodes, reduction of O2 in pri-
mary media may be achieved by two pathways, namely
peroxide pathway and hydrogen peroxide degradation to
form hydroxyl ion, causing an increase in pH at cathode and
Fig. 8 e Power density (mW m¡2) vs. time (min) graphs for production of caustic agents [116]. Even in Noble metal
different light intensities using monochromatic blue LED catalysts, the chance of hydrogen peroxide generation is
light (450e495 nm) (a) and monochromatic red LED light also high [23].
(620e750 nm) (b) as a light source for algal-MFC To overcome the negative impacts of pH changes on the
(Reproduced from Ref. [111] with permission). (For overall performance of MFCs, numerous buffers were used to
interpretation of the references to colour in this figure maintain optimum pH value [117,118]. But this process might
legend, the reader is referred to the Web version of this increase the net production costs. Accordingly, carbonate
article.) buffer is one of the cheapest, efficient pH buffer for com-
mercial applications [119]. Zwitter ionic buffers also showed

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12 international journal of hydrogen energy xxx (xxxx) xxx

advantages for their non-toxicity and non-interaction with MFC to serve as low-cost and efficient PEM. The low-cost
biochemical reactions [120]. ceramic materials have been used to prepare different types
of membranes. For example, clayware has been used as a PEM
Materials used in electrolyte and exchange membrane to obtain maximum power density (16.8 W m3) [135]. Clay-
ware have been also used as membrane/cathode with a
Materials used in the electrolytes can also affect the perfor- maximum power of 7.5 W m3 [136]. Polybenzimidazole
mance of MA-MFC and energy output. Several electrolyte membrane was shown promising results comparing with
materials have been studied including stainless steel, copper, Nafion in terms of energy output along with the cost and
gold and graphite carbon cloth in various sizes in an MA-MFC sustainability [133]. Recently, coconut shell was explored its
with Spirulina platensis based-anode [80]. Table 2 shows the potential as a PEM in MA-MFC. Coconut shells exhibited
energy production using different anode and cathode mate- higher water absorption more than 30%, which improve pro-
rials. The result showed that stainless steel revealed high in- ton movement through water molecules to the cathodic side
ternal resistance, which stuck electron transfer. Even though [134]. In the sediment MA-MFC, it can function without
copper recorded the shortest time to reach the maximum OCV membranes [137] or using different type of membranes to
value, it tended to oxidize. Maximum power density improve power generation such as hydrophilic polytetra-
(10 mW m2) was achieved by using gold-coated mesh as fluoroethylene membrane [90].
anode and graphite carbon cloth as cathode.
In some studies, a platinized cathode electrode has been
used as the primary electrolyte filmed with microalgae as an Algal cell density and chlorophyll content
O2 generator [28]. Nevertheless, using precious metals like
platinum is costly, which is not practical for the MFC scale up. Microalgal cell density at the anode is another critical factor
Moreover, the presence of sulfur, phosphate, and bicarbonate affecting bioelectricity generation; the maximum electric
in the algal cultivated medium or wastewater may inhibit the current was recorded at the lowest algal cell density
platinized cathode function [78]. Cathode material also plays a (5.94  106 cells/mL) using live a green microalga, C. pyr-
dynamic role in reducing cathodic reaction activation energy enoidosa, assisted-anode [80]. High algal density was reported
and boosting the overall rate of reaction [121,122]. Other au- to decrease the final power production, possibly by raising the
thors have focused on using inexpensive cathodic materials. O2 level and mass transfer problem. The power density and
In this context, two different carbon cathode electrodes open-circuit voltage (OCV) was influenced by Chlorophyll
namely a carbon fiber brush and plain carbon paper were contents of microalgae lining anode electrolyte [80]. It was
tested to induce power generations. Carbon fiber brush cath- also found that the OCV value of MA-MFC is increased by
ode showed a maximizes power density to 30 mWm2 cath- increasing Chlorophyll content up to 0.5 mg. Additionally,
ode compared to 4.6 mWm2 of plain carbon paper [123]. Zhai OCV is proportional to biomass area density and inversely
et al. [124] have used nanofiber on the electrode surface to with light intensity.
improve the performance of MFC. The maximum power On the other hand, power generation was reported to be
density of MFC was increased about 5 times (853 mW m2) increased with algal concentration in the cathodic chamber of
compared with the unmodified electrodes MFC. MA-MFC, since more O2 could be supplied by algae [138].
Moreover, the performances of MA-MFC can be greatly Recently, maximum power density (3.5 W m3) was achieved
improved by increasing the cathode surface area [125]. Zhang when the algal biomass of green algae Golenkinia sp. reached
et al. [29] used nickel foam/graphene (NF/rGO) as a cathode in the plateau under continuous operation on the 12th day, and
MFC and showed that graphene could enhance power gener- then it decreased [139].
ation (36.4 mW m2) with a decrease in the internal resistance
of microalgae-cathode MFC comparing to graphite plate Dissolved oxygen content
electrode (15 mW m2) [126], carbon fiber cloth (8.79 mW m2)
[71]. Dissolved oxygen (DO) generated during photosynthesis can
Proton exchange membrane (PEM) material also could significantly influence the power output of algal-MFCs by
affect the efficiency of MA-MFC in two ways, such as the decreasing the Coulombic efficiency and enhancing the
transfer rate of the protons [127] and the cost of the mem- degradation of aromatics compounds in the anode chamber
brane. Protons flow from anode to cathode requires higher [140,141]. To maintain the process, algae based-anodic
conductivity and low internal resistance, which can limit the chamber should be free of or at least has controlled the con-
passage of O2 and substrate [128,129]. The flow rate of chem- tent of dissolved oxygen. To overcome this problem, nitrogen
ical species depends on the potential gradient. Selective gas has been used or adding a highly concentrated salt solu-
permeability of protons is improved by the presence of tion [92]. In this case, microalgae should possess osmotic
negatively charged groups on the membrane. The selection of tolerance to keep cell functioning without damaging the cell’s
efficient membrane should be able to face internal resistance physiology.
[130], pH splitting [131], oxygen permeability [132] to reduce On contrary in the cathode chamber, increments of DO
the net cost of MA-MFC. Nafion membrane is one of the contents enhanced the reduction reaction rates at the cath-
commonly used membranes in MFC [133]. However, it has ode, indicating an increase in power output. Significant
many restrictions, including high cost, oxygen diffusion, improvement in the cathodic DO levels were observed during
cation precipitation, substrate loss, etc. [134]. Many advances the light period as a result of oxygenic photosynthetic activ-
have been reported in terms of new materials of PEM in MA- ities. Conversely, DO content dropped during night hours due

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international journal of hydrogen energy xxx (xxxx) xxx 13

to the consumption of the DO through microalgal respiration

[223]
[139]
[224]
[225]

[226]
[227]
[228]
[194]
[229]
[230]
[231]
[230]

[232]
Ref.

[24]
[25]

[80]
[18]
and stopping of photosynthesis. As a result, a higher electro-
genic activity was observed during the day that decreased at
night [85]. In this regard, operating MFC during spring gener-
ated higher energy output (57.0 mW m2) superior summer
Maximum power

(1.1 mW m2) owing to the higher oxygenic photosynthetic


density (W/m3)

rate of mixed microalgae and own DO content [85]. In fact,

6.5 m
0.852

14.11

0.168
termination of algal aeration declines both OD and electrical
24.9

3.93

4.35

5.94
386
144
3.5

6.6
7.6
46

10

45
current in the catholyte immediately [107].

8 Temperature

Temperature is one of the vital factors that affect electricity


generation of MFC. MFCs can effectually be operated over a

Single chamber (Electrochemical membrane bioreactor)


Single chamber (bioelectrochemical membrane reactor)
varied range of temperatures. Operating temperature effects
on power density, electrode potential, columbic efficiency,
Dual- Chamber (Ultrafiltration microbial fuel cell)

chemical oxygen demand removal and internal resistance of


MFCs [117]. In addition, its effect on the nature and distribu-
tion of the microbial community [142e144]. Liu et al. [145]
One anodic and two cathodic chambers

demonstrated that low temperatures (10  C) have a consider-


able effect on anode performance, nevertheless increasing the
temperature to 43  C had a primary effect on the cathode
MFC
type

potential when the MFCs have been operated at 37  C. The


maximum power density (7.89 W m3) was recorded at 37  C
double chamber MFC

Single chamber cube

and the lowest power density was achieved at 10  C


Single chambered
Single chambered

single chambered

(2.64 W m3), however, increasing temperature up to 55  C


PMFC cell (PMFC)

airlift type PMFC


Dual chambered
Single chamber

Single chamber

Single chamber
sediment MFC
dual-chamber

showed no steady power generation. The optimum internal


resistance was also observed at 37  C and increased by
Table 2 e Power generation capacity using different electrolyte materials microbial fuel cell.

decreasing or increasing than 37  C. Larrosa-Guerrero et al.


[146] studied the effect of temperature (from 4 to 35  C) on MFC
performance using wastewater in single and double-chamber
MFC. In a double chamber, low temperatures (4, 8 and 15  C)
showed significant improvements in COD removal. On the
Graphite fiber brush with Ti and graphite granules

contrary, these differences were insignificant at temperatures


of 20, 25, 30 and 35  C. In the case of a single chamber, the
maximum removal of COD and power density were achieved
at 35  C (94% and 8.1 mW m2cathode, respectively), while at
4  C the results were 50% less COD removal and 100 times
lower maximum power density. Adelaja et al. [147] detected
Stainless steel mesh air cathode

Stainless steel mesh biocathode


material
Cathode

that degradation efficiency and power density were both


Carbon mesh (Air cathode)

enhanced by approximately 200% at 40  C compared to MFC


Packed granular graphite
Air cathode-carbon cloth

Graphite felt biocathode

performance at 30  C but reduced sharply by 400% when


Packed bed air cathode

Stainless steel mesh


Catholyte: K Fe(CN)6

operating temperature was increased to 50  C using petroleum


carbon fiber cloth

hydrocarbon mixtures as a substrate. In general, the increase


Graphite felt

of power density with increasing of temperature may be due


carbon cloth

to the enhancement of the microbial metabolism, conductiv-


Platinum

Graphite
Ni-HFM

ity of the liquid solution and membrane permeability as well


as reduction of ohmic resistance [145,148].
Pt

Temperature also affects the performance of the MFC by


effecting on microorganism activity following an exponential
trend, consequently effecting on MFC power output by the
carbon based-nanomaterials
Graphite fiber brush with Ti

same trend. It is known that increasing temperature


Packed granular graphite

enhancing the microbial activity till optimum [149e151]. This


microbial activity can be detected by biofilm formation at the
Millilayer graphene
Pt coated Ti metal

Granular graphite
Anode material

Activated carbon

anode which influences anodic activity. Studying the effect of


Graphite brush

temperature on biofilm development displays that raising the


Carbon mesh
carbon brush
Carbon cloth

Graphite felt

Graphite felt

Graphite felt
carbon cloth

initial temperature of MFC has a significant impact on the


initial formation of anionic biofilm and on the time required
Gold

for starting. Higher temperatures (30e40  C for mesophilic


Pt

species) improve the biofilm stability decreasing the biofilm

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formation time and consequently a higher energy output wastewater [164], food waste [61,139], brewery wastes [102],
[152e155]. Lower and higher operation temperatures lead to a pharmaceutical wastewater [55,165] and even petroleum hy-
decrease in biofilm formation and MFC performance and drocarbon [166]. Different configurations were designed by
increasing the biofilm formation time due to reduce metabolic numerous workers. For instance, Jiang et al. [118] designed an
activity and to irreversible denaturation processes which may integrated system containing a membrane-free MFC with a
decompose biofilm [145,155]. Although different electrogenic PBR to remediate wastewater and generate bioelectricity. This
species had different optimum temperatures, the initial system depends on feeding wastewater to the up-flow MFC to
temperature is critical for biofilm development. Once the reduce COD, phosphorus and nitrogen along and generation
biofilm established, the microbial species were capable of of electricity. Cathodic effluent was used to feed microalgae in
adapting their metabolism functioning at different tempera- the external PBR for removing the residual nutrient content.
tures [146,152,154,156]. This setup achieved 99.3% phosphorus, 99.0% nitrogen and
78% COD removal with the maximum power density of
481 mW m3. Most recently, Scenedesmus abundance was
Application of MA-MFCs cultivated in PBR and coupled with MA-MFC for pretreatment
of pharmaceutical wastewater and bioelectricity generation.
Biofuel production In this system, wastewater firstly pumped to PBR for the first
pretreatment process then the pretreated wastewater was
Investigations have largely been done on simultaneous used as a feedstock for further treatment via MA-MFC and
microalgae growth and energy production by using algae in generate electricity. At the end of pretreatment, elimination
both cathodic and anodic compartments of MFCs. In 2015, efficiency reached to 95% of COD with a maximum voltage of
Gajda et al. [113] presented a closed operation cycle by feeding 0.740 V and a power density of 0.838 W m2, where maximum
the MFC with microalgae grown in the cathodic chamber, biomass reached to 0.71 g L1 in PBR and 0.78 g L1 in MA-MFC
obtaining 128 mW of power output. This set up simultaneously [55]. The treatment of kitchen wastewater was reported using
generates biomass and electricity from the algal biomass Ma-MFC consisting of living Synechococcus sp. and Chlorococcum
produced in the cathode of MFCs. sp as a cathode catalyst. The highest power density
Other workers have integrated bioelectricity with the pro- (41.5 mW m2) was recorded with Synechococcus sp. compared
duction of different kinds of biofuels. De Schamphelaire and to Chlorococcum sp. (30.2 mW m2). These integrated systems
Verstraete [114] developed a fully closed loop system to take the advantages of the continuous biotreating of different
convert the sunlight into biogas. The assembly depends on types wastewater along with producing electricity and
cultivate microalgae in a loop photobioreactor feed with the microalgal biomass with zero environmental impact.
CO2 produced by MFC. Concurrently, the produced biomass Although MFC is a promising approach for recovering the
was subjected as a substrate in an aerobic fermentor for energy and removing pollutants from wastewater, MFCs
biogas production. Moreover, the effluent of the anaerobic emitted a high amount of ammonia when ammonium-
fermentation was used as feedstock to enrich the anode abundant wastewater used for remediation such as swine
compartment with organic matter. This assembly achieved wastewater, dairy wastewater and animal slurry [167e169].
2e2.5 ton VS ha1 month1 of algal biomass and a biogas While the total nitrogen (TN) removal in the MFCs could reach
production of 500 N m3 g1 microalgae. 95%, ammonia volatilization contributed to around 60% of the
Biodiesel, bioethanol and bioelectricity generation were ammonia removal [168]. It has been found that during the
integrated into one system [159]. These biofuels coupled many electricity generation, the pH close to the cathode elevates
photobioreactors of C. vulgaris and a yeast MFC into an exist- which increases the conversion of ammonium ion (NH4þ) to
ing bioethanol production system. C. vulgaris captured the CO2 free ammonia to volatize via cathode [168,170]. High NH3
produced by the fermentation process in the cathode. Simul- emission might utterly diminish the application of MFCs for
taneously, algal biomass produced is used as a feedstock in wastewater treatment, according to the negative effect of NH3
the anode for fermentation to generate electricity. Interest- on climate change and air quality. In this regard, different
ingly, the high oil content of C. vulgaris was obtained that can efforts have been established to reduce NH3 emission without
be used for biodiesel production. Even algal biomass with low effecting on the energy generation. Recently, Li et al. [171]
lipid content and high carbohydrate contents could be utilized developed a novel Cu-blended 3D cathode which decreased
by pyrolysis or buried to different biofuel such as bioethanol the NH3 emission to 0.037 mg-N/L, which was 6.3% of that in
[31]. the activated sludge wastewater treatment plants. As well, the
good power density (14.4 W/m3) and high pollutants removal
Waste bioremediation (88.1% COD and 92.8% TN removal).

Several studies have demonstrated the potential application Desalination


of microalgae in the bioremediation process [25,160,161].
Microalgae could be incorporated in wastewater treatment by Microalgae based-cathode showed many advances in the
connecting MFC to a Photobioreactor (PBR), in which the desalination process in special fuel cells called Microalgae
released gases are exchanged. In fact, utilization of such toxic Assisted Microbial Desalination Cell (MA-MDC). MA-MDCs is a
and polluted substrates itself is a great benefit. Several types new, green and eco-friendly approach that desalinates
of wastes and wastewater could be used as the substrate for seawater efficiently along with bioelectricity generation.
MFCs such as sewage sludge, and urine [162,163], domestic Comparing to the traditional desalination techniques that

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international journal of hydrogen energy xxx (xxxx) xxx 15

need high-grade electricity and high operating cost, this in- vulgares [174]. A maximum power density of 0.75 W m2 was
tegrated approach can reduce the emission of greenhouse observed using static MA-MDC, but the maximum biomass
gases, as well as waste heat emission. As a consequence, new growth rate was 7 mg L1 h1 in continuous form. Interest-
renewable technology has been developed called bio- ingly, the removal rates of TDS and COD along with power
electrochemical systems. The principle of MA-MDC is density have increased by increasing TDS concentrations.
similar to that of MA-MFC with the addition of the desalina- Several studies that used algal-based-biocathode in MDCs
tion chamber located between the anodic and cathodic were summarized in Table 3. Based on these studies, it can be
chamber, to pull the anions and cations present through inferred that algal-assisted MDC can provide a renewable,
anion exchange and cation exchange membranes, respec- promising and sustainable technology for desalination of
tively thus desalinating the saline water occur (Fig. 9) [58]. wastewater with the potential power generation and algal
Microalga, Scenedesmus abundans, was used in the cathode biomass production.
chamber in MDCs that showed potential results better than
chemical cathode by increasing desalination efficiency and Other applications
COD removal from petroleum wastewater along with gener-
ating 654 mv of bioelectricity. The desalination efficiency A wide range of benefits can also be obtained by coupling
reached to 55.3% using 35 g NaCl L1 and 42.6% using 20 g NaCl MFCS with algal cultivation including, obtained algal biomass
L1 [172]. may consist of useful chemical compounds [175]. For instance,
Neethu et al. [31] designed a five-chambered MDC fed with algal-MFCs can produce biomass reached 900 mg L1 during
different concentrations of total dissolved solids (TDS) summer and 800 mg L1 in spring [176]. Microalgal biomass
(2.5 g L1 and 5.0 g L1) of saline water using C. pyrenoidosa as a can be increased under light and nutrient (nitrogen) stress
biocathode. MA-MDC operated with a low salinity level dis- [177] to get large biomass for various applications.
played the superlative performance with a maximum power Pigments are another by-product from algal-MFCs. Chlo-
density of 45.52 mW m2 and 71% desalination efficiency as rophyll content has been increased from 7.21 mg mg1 to
well as 78% COD removal more than the air cathode MDC. The 15.61 mg mg1 with operating time [176]. The chromatographic
influence of light availability and the electron-donating pro- fraction techniques confirmed the presence of chlorophyll a,
cess at anode were evaluated on MDCs performance [173]. The b, lutein, canthaxanthin, and b-carotene in algal pigment
results showed that microalgae perform improved under [175]. It has been observed that carotene content has been
natural light/dark cycles with no effect of COD concentrations. boosted under higher light intensities by inducing the car-
The performance of three different MA-MDC configurations otenogenesis process [177].
were studied (static, continuous and photobioreactor) using C.

Fig. 9 e Schematic configuration of Algal desalination MFC (Algal-DMFC).

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16 international journal of hydrogen energy xxx (xxxx) xxx

Table 3 e Summary of three chamber algal-microbial desalination cells with desalination rate, chemical O2 demand
removal and maximum power output.
Microalgae Van:Vdesal Type of Salinity Desalinity rate COD removal Pmax (mW m3) Ref.
:Vcaa wastewater level (g L1)
Chlorella vulgaris 1:1:1 Dairy 35 52% e 20.25 [233]
C. vulgaris 2:2:1.4 Sludge of treatment plant 64.2% 68.02% 1.1 [234]
C. vulgaris 0.9:1:0.5 Synthetic 40% 63.3% 151 [173]
C. vulgaris 1.3:1:1.3 Synthetic (different conc.) 35 32.2% 64% 675 [174]
Nannochloropsis salina Rumen 17.5 79% 85% 384 [235]
a
Van Volume of anode chamber, V desal: Volume of desalination chamber, Vcat: Volume of cathode chamber.

with cyanobacteria showed the maximum power density of


Limitations and challenges in MA-MFCs 0.072 W m2 with a substrate degradation rate of 0.607 kg COD
m3 d1. The presence of mediating compounds in the cya-
MA-MFCs have many advantages, including lower costs, high nobacterial acidic fermentation broth increased the chance of
valuable biomass, high CO2 sequestration, mild operational electron transfer to the anode electrolyte. Another study used
conditions, resistance to harmful materials, high reaction rate a partly digested algal suspension and the rest substrate was
etc., making the MA-MFC an efficient and sustainable process. fed to the anodic compartment of the MFC [158]. The partly
Despite all these benefits, it still has some restrictions that anaerobic digestion increased the electron donors availability
limit its commercial application that needs further improve- for electrochemically active bacteria [158].
ment [133,178]. General limitations include a slow activity of Different studies have enriched algal culture with elec-
autotrophic microalgae when compared with heterotrophic tricigens for maximizing MA-FCs performances. Electrogenic
species thus affecting the whole MA-MFC operation; energy microalgae can generate electrical energy and using less en-
loss caused by high potential; open-air cathode increases the ergy via photosynthesis process compared with bacteria.
resistance of charge transfer; inferior performance of bio- Despite microalgae have complex electron transfer networks,
cathodes compared to chemical cathode in terms of power they are primarily adapted for light-harvesting and not for
generation; influenced by sunlight intensity in an open-air electron shuttling [185]. Once electron generated from
operated cell; algal biomass harvesting problems in large photosynthesis, many electron sinks are available to protect
scale production, etc. that encounter scale-up application of cyanobacteria from light stress [186,187]. However, these
this technology [179e181]. On the other hand, the long-term electron pathways are not recommended and wasteful alter-
operation of MA-MFC results in voltage decrease due to the natives for electrons in terms of electrogenic activity. There-
basic microenvironment in the cathode side. The passage of fore, some electrogenic bacteria were used to improve the
organic materials from the anode to the cathode may reduce electron output and convert light energy into electrical energy
the MFC and biocathode performance by their toxic effect on with high efficiency. Addition of electrogenic Pseudomonas sp.
the microalgae at the cathode side, and converting autotro- strain WJ04 to cyanobacterium Synechocystis sp. PCC6803 in
phic biocathode to heterotrophic ones [30,182]. Suspended anodic side of double chamber MFCs increased the voltage
organic compounds, also, tend to increase algal culture output by more than 12-fold compared to the pure culture of
turbidity and reduce light penetration into the culture [166]. Synechocystis sp. PCC6803, meaning that strain WJ04 contrib-
All these bottlenecks have limited to make algal MFC a prac- uted to the increased output energy. This owning to the pos-
tical and commercial technology. itive effect of Pseudomonas on the growth of Synechocystis by
An important question is how the energy output can be improving the electron output and the photosynthesis rates
enhanced to obtain a cost-effective MA-MFCs. There are many by regulating algal genes and metabolite production [188]. It
possible approaches to increase power recovery of algal MFCs has also been found that addition of electrogenic Geobacter
that will be illustrated in the following points: sulfurreducens to Chlamydomonas reinhardtii based-anode could
Increased substrate availability and organic load rate (OLR) achieve a power-conversion efficiency of 0.1% [83] three-time
is one of the applicable options to enhance power production. more than the average of power-conversion efficiency in
Electrochemically active microbes at the anode side can phototrophic MFC [189].
oxidize more organic matter than supplied. Thus, increasing Comparing to other land plants, Unicellular microalgae
the substrate availability and OLR will increase the biode- have a highly productive rate and photosynthetic efficiencies.
gradable rate as well as the electron flux [29]. OLR is propor- But this efficiency can be reduced by poor kinetic coupling
tional to the power density [23]. As it was observed that among light-harvesting, photochemical, and electron transfer
increasing the OLR from 1.92 to 3.84 g L1 d1 increased the processes [129,190]. The photosynthetic efficiency can be
power density from 1.88 W m3 to nearly 3 W m3 [183]. boosted in different ways such as regulating the light-
Zhao et al. [134] used four different feedstocks namely harvesting antenna, manipulating growth conditions, and
acidic fermentation broth of cyanobacteria, raw cyanobac- reduction of antenna size per reaction center complex
teria, sodium acetate and glucose. Acidic fermentation broth [191,192]. Increasing light intensities can greatly increase the

Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
international journal of hydrogen energy xxx (xxxx) xxx 17

photosynthetic efficiency by reducing the cell shading and electron donor at the anode. Living C. vulgaris at the cathode to
allow light to penetrate to more depths. The reduction in provide oxygen as an electron acceptor and served as a lipid
pigment content per algal cell and decrease the antenna size source for biodiesel production. The MFCs performed perfec-
are targets for optimizing the photosynthetic efficiency under tively in all facets including energy recovery (11.53 kW m3),
mass culture [190,193]. algae productivity (0.09 kg m3d1), and cost of operation
Several studies used different promoting compounds to ($11.225).
increase electron flow in the anodic chamber. One of these
compounds is 4-nitroaniline 4NA observed that when C. vul-
garis cells were exposed to 20 ppm 4NA, the open-circuit
voltage would begin to enhance at about 30 min and reach Conclusion
the maximum after 130 min at 38 mV. This according to the
addition of 4NA increased the algal cell permeability and MA-MFC offers a smart technology for generating
decrease the resistance during the electron transfer from algal bioelectricity, as it can play as a bio-anode or biocathode in
cell to the anode electrode, resulting in increased the OCV in MFC with low operational costs. The activity of MA-MFC de-
MFC [92]. pends on sunlight, valuable byproducts and biomass. One of
Several reports observed that the addition of nitrogenous the significant aspects for MA-MFC is the dependence of the
compounds on the surface of anode increases the N/C ratio of recycling concept, where algal biomass can act as a source of
the surface that enhanced the bacterial attachment, the sur- nutrients in the anodic compartment, while the evolved gas
face hydrophilicity and indirectly the MFCs performance from the anode can be fed by algal cathodic side in the same
[194e197]. Cheng and Logan [145] showed that the ammonia MFC. Overall energy out from MA-MFC can be affected by
treatment of carbon cloth anode improves the positive charge, various factors, including pH, OD, electrolyte materials, etc.,
as nitrogen-containing surface functional groups is formed an which should be established as the optima to achieve
anode surface, which is conducive to the accumulation of maximum performances and high output. Moreover, the
microorganisms and increased the electron flow to the anode. generation of bioelectricity by MA-MFC provides opportunities
The methods of increasing the nitrogen content of anode to integrate it with the production of biodiesel, wastewater
electrode, including ammonia, heat or nitrogen dioxide treatment, desalination, and other applications, since micro-
treatment, is a way to improve MFC performance through algae also hold potentials for these approaches. Nevertheless,
anode modification, indicating that the control of nitrogen researches efforts are needed to operate this technology effi-
content is vital to achieve high performance of MFCs [198]. ciently on a large scale. This may include designing a more
Recently, two nitrophenyl compounds namely 4-nitroaniline efficient coupling system for reducing cost and increasing
and 4-nitrobenzenediazonium tetrafluoroborate were used conversion efficiency.
to increase of nitrogen content on the anode surface. 4-
nitrobenzenediazonium tetrafluoroborate showed the best
result in terms of power output and MFCs performance [194]. Declaration of Competing Interest

The authors declare that they have no known competing


Current status of MFC financial interests or personal relationships that could have
appeared to influence the work reported in this paper.
Biorefinery concept and large-scale application are the most
futuristic ways to augment MFC applications. Future research
should establish to develop low-cost large-scale MFCs for the Acknowledgements
removal of organic pollutants, nutrients, xenobiotic and
recalcitrant materials from wastewaters and powering low This work was supported by the National Natural Science
energy devices. For achieving these goals, economical elec- Foundation of China (Grant No. 31972042, 31950410550 and
trodes, efficient catalysts and proton exchange membrane 31571806) and High-level talents project of Six Talent Peaks in
(PEM) should be produced from renewable waste-based re- Jiangsu Province of China (Grant No. SWYY-018).
sources to recover the waste-derived material efficiently, to
reduce the manufacturing cost of MFC [199]. Biochar is one
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bioelectricity, International Journal of Hydrogen Energy, https://doi.org/10.1016/j.ijhydene.2020.06.251
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