Elshobary (2020) Recent Insights Into Microalgae-Assisted Microbial Fuel Cells For Generating Sustainable Bioelectricity
Elshobary (2020) Recent Insights Into Microalgae-Assisted Microbial Fuel Cells For Generating Sustainable Bioelectricity
Elshobary (2020) Recent Insights Into Microalgae-Assisted Microbial Fuel Cells For Generating Sustainable Bioelectricity
ScienceDirect
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.
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
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.
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international journal of hydrogen energy xxx (xxxx) xxx 5
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 !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 O!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
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
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
Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
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10 international journal of hydrogen energy xxx (xxxx) xxx
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]
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
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 11
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
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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
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 13
[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
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
single chambered
Single chamber
Single chamber
sediment MFC
dual-chamber
Graphite
Ni-HFM
Granular graphite
Anode material
Activated carbon
Graphite felt
Graphite felt
Graphite felt
carbon cloth
Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
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14 international journal of hydrogen energy xxx (xxxx) xxx
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).
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 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.
Please cite this article as: Elshobary ME et al., Recent insights into microalgae-assisted microbial fuel cells for generating sustainable
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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.
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
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
18 international journal of hydrogen energy xxx (xxxx) xxx
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