Algal Biocathodes

C H A P T E R

3.7 Algal Biocathodes C. Nagendranatha Reddy, Ramesh Kakarla, Booki Min Department of Environmental Science and Engineering, Kyung Hee University, Yongin-si, Republic of Korea

3.7.1 INTRODUCTION Clean forms of energy and water are utmost needs of society that helps to maintain environmental homeostasis and sustenance. Commercial exploitation of nature and its resources viz., rapid industrialization etc. for economic growth, resulted in negative connotation of accompanying environmental pollution thereby affecting the whole ecosystem in a direct and indirect way. Today, most of world’s energy (w80%) consumed is sustained by the extraction of fossil fuels [1,2]. The rapid increase in population, demand for commodities, increase in sophistication of technology for efficient and swift extraction of natural resources etc., has created a huge demand for energy in all sectors that led to the unsustainable extraction of fossil fuels [3]. Apart from sustainable energy issues, excessive usage of fossil fuels in various sectors, discharge of waste in huge quantities by the increased human population and economic growth becomes an increasing concern that needs to be addressed immediately. Hence, a multifaceted approach of integrating sustainable and eco-friendly technologies in a sequential closed loop approach provides a step toward circular bio-economy [4,5].

3.7.1.1 Principle of MFC A microbial fuel cell (MFC) is an electrochemical system that utilizes the activity of various biocatalysts (microorganisms), facilitating the direct and efficient conversion of a variety of organic substances (substrate) to electrical energy (bioelectricity) through a cascade of oxidation and reduction (redox) reactions [6e9]. It has the inherent advantage of coupling both fuel cell and biological treatment processes in a single bioreactor. The MFC system is characterized by the presence of electrode assembly, comprising an anode and cathode necessary for carrying out oxidation and reduction reactions, respectively, and separated by a

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membrane [10,11]. The redox reactions responsible for the overall activity of an MFC are determined by individual half-cell potentials, which are in turn dependent on many factors viz., electrode material and size, electron transfer mechanisms, and the irreversible electrode reactions etc. [12]. Based on the assembly of anode and cathode, the bioreactor can be either single or double chambered. The conventional MFC design and structure were modified according to the present state requirement [13,14]. The overall performance of an MFC is dependent on various factors viz., type and composition of wastewater, microbial community, bioreactor size, configuration, electrode materials, catholyte, biofilm or suspended mode of operation, microenvironment, the distance between electrodes, and varying operating conditions etc. [15e17]. The potential of generating value addition by utilizing carbon/organics from waste/wastewater makes the MFC technology a sustainable process. The applications of MFCs include wastewater treatment [18], bioelectricity generation, value-added products generation etc. [19e21]. The MFC was able to generate bioelectricity by treating various wastewaters viz., domestic, textile, pharmaceutical, chemical, lignocellulosic, heavy metale contaminated wastewaters etc. [22]. To meet the present state requirement, MFCs have been classified as stacked and multielectrode assemblies, sediment type, benthic, submersible, and plant-based MFCs [8,13,23e29] to improve power generation, applicability and feasibility etc. The MFC technology to treat wastewaters has several advantages compared with the conventional treatment modes yet suffering from inborn limitations. A significant improvement is yet to be made in the MFC design, electrode materials, and operation conditions with enhanced electricity generation [30].

3.7.1.2 MFC Limitations Some of the limiting factors for MFC operation are partial substrate oxidation, electrochemical losses, reactor configurations, biocatalyst type and activity, and availability of terminal electron acceptor (TEA) in different phases. In field scale, the applicability of MFC is still suffering from several limitations, including high costs, configurations, and fouling of membrane and electrode materials [31]. In MFC the significant role in enhancing the overall performance is attributed equally to two half cells. Regulating the electrochemical behavior of MFCs toward higher power output and heightening the transfer kinetics at the anode can be made possibly through the optimization of circuitries and by varying the phase of TEAs available. The controlled electron flow through the circuit for recovering maximum power densities is dependent on the proton movement across the proton exchange membrane, which is further interdependent on the TEA. To overcome the limitation of low Hþ mobility, the availability of an effective TEA is essential in the cathode chamber that enhances the driving force for drawing the electrons toward higher reduction [32e35]. The electronaccepting potential varies under liquid and gaseous phases, which also influences the other governing factors of the MFC such as electrode potentials, redox mediators, electron kinetics, power production, etc. TEAs such as oxygen (O2), nitrate, sulfate, iron, metals, etc., could act as effective electron acceptors owing to their high reducing capacity [36e38]. The presence of effective biofilm on anode electrode and good reduction potentials during MFC operation towards enhanced performance has been reported previously [39].

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3.7.1.2.1 Cathodic Reaction Limitations During recent periods, more focus is being paid on cathodic limitations to achieve high efficiency from MFCs [36,40]. Generally, the cathodic reduction of O2 to water by utilizing Hþ and e obtained from anode chamber drives the potential toward bioelectricity generation. The MFC cathodes can be classified into abiotic and biotic cathodes. Abiotic cathodes catalyze the cathodic reactions without the involvement of any living organisms with or without the aid of a catalyst. Whereas, the biocathodes are the cathodes that make use of living organisms for their cathodic reaction as catalysts, and for this purpose a wide variety of organisms were implemented, including bacteria, yeast, and algae. Kinds of abiotic cathode include chemical cathode (ferricyanide), the aerated cathode (dissolved O2 cathode), and air-exposed cathode [35,39]. The drawbacks pertaining to the above-mentioned type of cathodes are complex design of MFC for an air-exposed cathode, mechanical aeration cost for the aerated cathode, and regeneration capability of chemical cathode thereby leading to secondary pollution. The O2 serves as an ideal TEA due to its nontoxic effect and easy availability in the atmosphere. Whereas the ferricyanide is toxic and may have adverse effects on the biocatalyst and should be replenished frequently [19]. The economic and adverse limitations of using chemicals, expensive cathode materials (eg. Platinum), and continuous aeration of catholyte in field scale operation would decrease the net energy of MFC operation. The amount of TEA available is always important for better cathode performance and MFC performance. The cathode material also plays a vital role in reducing the cathodic reaction activation energy and increasing the overall rate of reaction [41,42]. The cathodic reaction can be classified into either aerobic or anaerobic reductions based on the availability of final electron acceptor source. In anaerobic conditions generally pollutants such as nitrates etc. will act as a final electron acceptor while O2 is the TEA in aerobic cathodes [43,44]. The principal electrochemical reaction at the cathode electrode is the reduction of O2. The number of O2 molecules that are involved in cathode reduction process is a determining step in maintaining higher cathode potentials. The most commonly employed oxidant for MFC cathode is O2 due to its ubiquity, high standard redox potential of 0.82 V, inexhaustibility/availability, etc. [45]. The use of higher O2 (dissolved oxygen [DO]) levels has several benefits such as (1) increased MFC cathode potentials and power densities [46], (2) decreased cathode over potentials as most of the cathode catalytic sites are involved in reaction, and (3) reduced mass transport and overpotentials on cathode surface [31,47]. Most bacteria are preferentially inclined toward transferring electrons to available O2 compared with other TEAs since it provides the maximum energy harvest. Also to maintain the maximal harvest of electrons from the bacteria, the cathode surface area should be in optimal contact with sufficient O2 for conducting and offering maximum oxygen reduction reaction [35,48]. However, in practice, cathode reduction potential with O2 is lower than the theoretical value. General open circuit potential of an air cathode is around 0.4 V vs Ag/AgCl, with an approximate short circuit potential of 0.25 V having a platinum (Pt)-coated cathode electrode as previously reported [49]. The reduction of O2 to form water needs four electrons (Eq 3.7.1); however, this process could be hindered with the formation of hydrogen peroxide (H2O2) with use of two electrons. The reduction potential of this H2O2 formation (0.695 V vs NHE) is bit lower than the redox theoretical potentials of water formation reaction (Eq. 3.7.2).

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The formation of H2O2 at cathode could result in degradation of cathode materials and membranes of MFC. However, the formation of H2O2 might act as a disinfectant in keeping the cathode and membrane free from microbial contamination [50]. O2 þ 4Hþ þ 4e ¼ 2H2 O

(3.7.1)

O2 þ 2Hþ þ 2e ¼ H2 O2

(3.7.2)

The use of cathode in abiotic form without any catalytic activity have a bit higher internal resistance compared to anode electrode that makes use of conductive bacterial biofilm. In this regard several inventions have been made to increase its conductivity by implementing high surface area cathode electrodes including carbon fiber brush [51], activated carbon and coating electrodes with metal catalysts including Pt, MnO2, Co, CoTMPP, MnPc, CoTMPP, MnO2, MnOx, and Co/Fe/N/CNT [52,53]. In fact the use of a metal catalyst can possibly increase the operation cost of MFC and become inactive in long-term operation or with the presence of sulfur, bicarbonate, and phosphate while operating with wastewaters [51]. During operation of MFCs, the voltage generated is less when compared with predicted thermodynamic ideal voltage due to overpotentials. The extent of these overpotentials losses vary from one system to another. The three different overpotentials or irreversible losses that affect the performance of MFC bioreactor are activation, ohmic, and mass transport losses. These losses are the result of voltage required to compensate for the current lost due to electrochemical reactions, charge transport, and mass transfer processes that take place in both the anode and cathode compartments [44]. Hence, anode and cathode overpotentials collectively limit the performance of MFC, and this varies with one bioreactor to another. The overall performance of the bioreactor can be improved by optimizing both the anode and cathode chambers. The cathodic compartment losses can severely affect the performance of MFCs in spite of proper anode functioning and pose a major challenge for research and development in the area of MFC. The activation losses can be reduced by adding mediators and catalysts (metal based or biocatalysts) and optimizing cathode surface area and other operational conditions [43,54e58]. For minimizing cathodic ohmic losses, space between electrodes should be reduced, and the conductivity of catholyte electrode materials and membranes should be increased [37,57,59]. Various studies conducted reported the improved performance of MFC by optimizing different operating conditions, electrode material, cathode compartment geometry and even distribution, and high bulk concentrations of oxidant that could be obtained by minimizing the overpotential losses [44,60,61].

3.7.1.3 Introduction of Biocathodes in MFC Operation The limitations that are put forward (nonrenewable, environmental toxicity, increased material costs, high over potentials for O2, etc.) with use of chemical and metal catalysts for cathode have made researchers think of alternative possibilities led to the utilization of biocathode.

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The main purpose of using biological organisms for catalysis is to reduce the cost of operation, to avoid chemicals and expensive metal catalysts with the sustainable operation, and to mediate the reduction of an oxidant either directly or indirectly accepting electrons from the cathode. Moreover, the implementation of biocathode has several advantages compared with abiotic cathodes, including microorganisms in the cathode mimic the metal catalysts and artificial electron mediators while assisting the electron transfer from anode to cathode, no need for expensive and toxic oxidative chemicals, simultaneous removal (reduction) of toxic compounds from wastewaters such as Fe(III), nitrate, and Mn(IV) compounds [62]. In some studies generation of bioalcohols and biogas was also reported with use of anaerobic biocathode with applied potentials [63]. If in case of algal biocathode, algae can provide O2 along with nutrient removal and biomass generation [64]. The involvement of these living organisms in the cathode reaction can be a direct (attached bacteria) [65] or indirect (with mediators) [66] approach. Cournet et al. [67], and Freguia et al. [68] had implemented heterotrophic microorganisms capable of donating electrons for reduction of O2, but they encountered several problems, including having a lower reduction potential compared with O2 reducing reactions as well as the need to provide supplemental O2, substrate, and nutrients. These drawbacks must be overcome to achieve long and sustainable operation of MFCs. Whereas, the anaerobic biocathodes require specific potentials along with electron acceptors such as nitrate or sulfate, and the reduction potential was lower compared with O2 reducing reactions [65]. In fact, a potential way is to use sustainable organisms that can produce O2 for cathode reduction is crucial. The only organisms that can produce O2 on this planet earth are photoautotroph’s considerably chlorophyll-containing organisms, including plants and algae [69]. The use of plants in the cathode chamber is not quite comfortable, and optimizing and controlling the growth were also difficult, while the algae are small in size and can grow rapidly in the broad range of climatic variations. Various biocatalyst used in biocathodes of MFC are bacteria [4,70e74], photosynthetic bacteria [75e78], white rot fungus [79], algae [78,80e84] etc.

3.7.2 ALGAL BIOCATHODES 3.7.2.1 General Introduction and Role of Algae in Cathodic Reactions The concept of generating O2 on the cathode chamber by utilizing light energy was first reported by Berk and Canfield, [85]. They used Rhodospirillum rubrum and blue-green marine algae on anode and cathode, respectively, to generate a maximum open potential of 0.96 V and a short circuit current of 750 mA/m2 under illumination. Recently, research on biocathodes is blooming as an effective and potential solution to eliminate cathode aeration and to overcome the limiting aspects of the O2 reduction reaction rate in the cathodic chambers of MFC [86]. Keeping in mind about the future energy sources to be renewable and carbon neutral, algae (both micro and macro) have attracted considerable interest as a potential feedstock for a bio-based economy [87e89]. The technology of integrating algal photosynthesis with MFC for in situ generation of O2 is known as photosynthetic MFC (PMFC). Unlike catalytic efficiency of heterotrophs which is limited by low cell yield and applicability, photoautotrophs serves as potential alternative in the biocathodes of MFC due to their inherent

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advantages of versatile and fast growth (doubling periods as short as 3.5 h), food security point of view (no competition with arable land and all-round the year harvesting), aqueous media growth, carbon dioxide (CO2) fixation, efficient converters of solar power, uptake of nutrients (NPK; Nitrogen, Phosphorus and Potassium), generation of O2 (to act as TEA), circumventing the utilization of exogenous and unstable mediators and precious catalysts, high lipid content (oil content in the range of 20%e50% dry weight of biomass), no requirement for pesticides or herbicides, and production of value addition (biomass, proteins, biodiesel, biofertilizers, pigments, nutraceuticals etc.) [90e95]. Hence, algal biocathodes provide the continuous and sustainable way of providing O2 by the photosynthetic mechanism as they contain chlorophyll organelles to utilize sunlight and sequester carbon from both aqueous and gaseous phases [96]. Algae assimilate pollutants into cellular constituents such as starch, carbohydrates, lipid, proteins, etc. thus achieving treatment in a more sustainable and environment-friendly way [97]. The aforementioned advantages of utilizing algae have garnered much prominence in bioeconomy domain, making it feasible for real-world applications and development of alternate biofuels (Fig. 3.7.1). However, the cost of algal growth and biomass harvesting is limiting the technology at large scale [88,91,94].

3.7.2.2 Mechanisms for CO2 Sequestration by Algae The increase in atmospheric CO2 concentrations has led to climate change, which in turn has adverse effects on overall nature and ecosystem. As reported by the International Energy

FIGURE 3.7.1

Schematic representation of photosynthetic biocathode in microbial fuel cell operation.

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Agency, the quantity of CO2 released in 2007 due to anthropogenic activities was 28.8 Gt, which is expected to increase to 40.3 Gt by 2030 and to 50 Gt by 2050, if proper precautions are not taken [5,98]. Hence, research is being focused on effective sequestration of CO2 from the atmosphere. Though there are various CO2 capture and storage techniques available and practiced, they have the limitations of huge costs which in turn is not economically feasible. Thus, the biological sequestration methods act as the viable method of sequestering CO2 along with simultaneous value addition. This method of bio sequestering and fixing atmospheric CO2 and synthesis of bio-based products could lead to important breakthroughs in CO2 capture and utilization methods and paves a way for carbon neutrality. The biological mechanisms that aid in CO2 fixation and sequestration by algae are photosynthesis and CO2 concentrating mechanisms (CCMs) [5,99,100]. 3.7.2.2.1 Photosynthesis Mechanism Algae act as the efficient sink for CO2 by carrying out oxygenic photosynthesis and play a significant role in global carbon and nitrogen cycles as primary producers. Photosynthesis is the process of CO2 sequestration using water and light energy to generate a variety of products viz., fuels, polyunsaturated fatty acids, nutraceuticals, chemicals pigments, dyes etc. The algal metabolic activity can uptake inorganic carbon in the presence of carbonic anhydrase. From the pool of bicarbonate entering the plastid of the cell, carbonic anhydrase provides CO2 to ribulose 1,5 bisphosphate carboxylase-oxygenase (RuBisCO) [5]. The light-harvesting center and chlorophyll harness the energy from electron transport chain on the thylakoid membranes of chloroplasts and store it in the form of nicotinamide adenine dinucleotide phosphate hydrogen (NADPH) and adenosine triphosphate (ATP) to be further consumed for carbohydrates synthesis in the light-independent stage. The two reaction centers, viz., photosystem II (PSII) and photosystem I (PSI), on thylakoid are specialized to absorb the light of wavelength 680 and 700 nm, respectively. They are connected to several electron carriers such as plastocyanin, cytochrome b6f, plastoquinone etc. that are arranged in the order of increasing redox potential to allow the flow of electron from negative to positive redox potential. With the light absorbed at 680 nm, the water is split into Hþ, e, and O2 molecules at oxygen evolution complex in PSII (Eq. 3.7.3). The O2 formed will escape, while Hþ accumulates in the lumen of the thylakoid membrane thereby creating proton gradient to form ATP. The excited electrons at PSII travel to PSI and it further gets excited to reduce ferredoxin (Fd) [101]. Reduced Fd transfers its electrons to the ferredoxin nicotinamide adenine dinucleotide phosphate (NADP) reductase, which catalyzes the formation of NADPH using NADPþ and Hþ coming from the lumen. The production of 2 mol of NAD(P)H requires eight photons and 2 mol of water as shown in Eq. 3.7.4 [102]. The overall photosynthetic reaction of CO2 fixation to generate O2 molecules is shown in Eq. 3.7.5. 2 H2 O ƒ! 4 Hþ þ 4 e þ O2

(3.7.3)

2 H2 O þ 2 NADP þ þ8 Photons ƒ! O2 þ 2 NADðPÞH þ 2 Hþ

(3.7.4)

6 CO2 þ 6 H2 O ðin presence of light and chlorophyllÞ ƒ! C6 H12 O6 þ 6 O2

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(3.7.5)

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3.7.2.2.2 CO2 Concentrating Mechanisms The CCM is the biological adaptation of photosynthetic microorganisms to augment photosynthetic activity by increasing inorganic carbon levels when there are low concentrations in the atmosphere and environment. CCMs are based on the biochemical mechanisms that increase the CO2 concentrations for RuBisCO by the process of particular cellular compartment acidification. Modulating CCMs may be crucial in the energetic and nutritional budgets of a cell, and a multitude of environmental factors can exert regulatory effects on the expression of the CCM components. Among various methods of concentrating CO2, few mechanisms include active transport of inorganic carbon, C4 photosynthesis, and CO2 concentration following acidification in a compartment adjacent to RuBisCO (Fig. 3.7.2). The photosynthetic microorganisms have difficulties to acquire CO2 from the atmosphere. The three different challenges faced by algae are low affinity of RuBisCo for CO2 at atmospheric levels, diffusion of CO2 in an aqueous solution is 10,000 times slower than the diffusion of CO2 in air and significant fluctuations in inorganic carbon levels and pH [100,101,103e105]. These factors limit the CO2 availability to the RuBisCO to discharge carboxylase activity of fixing CO2 into cellular components. In fact under the normal atmospheric condition, RuBisCO is only half saturated with the CO2. Mostly all the algal cells have developed CCM mechanisms to enhance the local partial pressure of CO2 (nearly Periplasmic space

CO2 CO2

H+ + HCO3-

Carbonic anhydrase

H+ + HCO3-

Cytosol CO2 + H2O

Carbonic anhydrase CO2 + H2O

Chloroplast

Ferredoxin NADP reductase

Ferredoxin

Lipid bilayer

Cytochrome b6f Plastoquinone

Plastocyanin

Oxygen evolving unit

FIGURE 3.7.2

Carbon dioxide sequestration mechanisms via. photosynthesis mechanism.

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1000 times more than the outside pressure) near the RuBisCO. Depending upon the
pH of the liquid medium, the CO2 is stored in the form of dissolved CO2, carbonate CO3 2 , HCO3  , and carbonic acids (H2CO3). The affinity constant (Km) of microalgae (C. reinhardtii) for CO2 is generally w20 mM. Most of the algal species were found to assimilate both CO2 and HCO3  [102].

3.7.2.3 MFC Operation With Algal Biocathodes Several studies reported the use of algae as cathodic biocatalyst in order to obtain the maximum benefits in PMFC operation. In this chapter, algae as cathodic biocatalyst are evaluated in detail. MFCs with algal biocathodes are one of the advanced technologies that make use of photosynthesis and anaerobic substrate oxidation process (in dual-chambered systems only) in the cathode and anode chambers, respectively. The photosynthetic algae in the cathode chamber utilize atmospheric CO2 or carbon from wastewater and sunlight via photosynthesis process for their growth and also for O2 byproduct generation. The in situ generated O2 acts as a TEA and helps in replacing the conventional mechanical aeration methods and is considered as the more sustainable alternative in both economic and environmental terms [45]. The overall process of reactions occurring in algal biocathodes is depicted in Fig. 3.7.3. The configuration and integration of processes play a significant role in defying the activity of biocatalyst in response to bioelectricity, treatment of various waste/wastewater as substrates, and value addition. These configuration types aid in long-term performance of bioreactors in integration with other processes. 3.7.2.3.1 Standalone Process (Dual Chambered) The dual-chambered MFC consists of two chambers separated by a membrane. This configuration uses algal photosynthesis as the source of O2 in the cathodic chamber and is considered the most common design. The algae aid in CO2 fixation in the presence of sunlight

Substrate/Waste

Inorganic CO2

Organic COD in wastewater Nutrients (NPK) in wastewater

Algae CO2 FixaƟon

H +e

O2 With Processing

Biomass Growth COD DegradaƟon

20 Products

10 Products

Biomass Without Processing

Nutrients Uptake

Treated water

H2O Biodiesel, Polyunsaturated FaƩy Acids (PUFA), Omega 3 faƩy acids, Pigments, NutraceuƟcals, de-oiled biomass as substrate etc. BioferƟlizer, Food, Feed and substrate DomesƟc or IrrigaƟonal purposes (Low Carbon, nitrogen and phosphorus)

Photosynthesis

FIGURE 3.7.3

Functioning of algae in biocathode of microbial fuel cell for waste treatment and simultaneous

value generation.

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and have a vital influence on the overall performance of the bioreactor along with the reduction in the overall costs involved [94]. Algae can be used as a photosynthetic organisms in either anode or cathode or both chambers with sludge or chemical cathodic catalyst in other chambers depending on the objective of the study [106,107]. PMFC using algae as O2 supplier was evaluated for maximum electricity generation (0.21 V; 30 mW/m2) thereby demonstrating that the O2 supplementation from algal photosynthesis is beneficial compared with general atmospheric air sparging with less energy consumption [51]. In another recent study reversible anode and cathode responsible for both anodic and cathodic electron transfer were developed by using an undefined mixed culture containing microalgae. The maximum power density of the reversible bioelectrode during cathodic and anodic currents was 3.1 and 41 mW/m2, respectively, with coulombic efficiency (84%) of O2 reduction at the biocathode. By determining the function of bioelectrode with the presence of illumination and O2 concentration, the MFC generated continuous power, solving pH membrane gradient problem [82]. Moreover, a forced biofilm formed by mixed culture of oxygenic phototrophs (cyanobacteria Synechococcus leopoliensis, Anabaena cylindrica, and the algae Chlorella pyrenoidosa) on carbon veil electrodes produced a constant voltage upon illumination, thereby proving the power generating capabilities of photosynthetic microorganisms. The cultures were used in synergistic interaction as C. pyrenoidosa and S. leopoliensis were highly active and fast growing, while A. cylindrica facilitates the anchoring of the two other strains in the cellulose matrix. The results suggested stable voltages of 6.58 mW/m2 generation by the projected surface area of biofilm with a clear indication of biofilm and illumination influence on the enhanced performance [108]. González del Campo et al. [81], also evaluated the mediator-less algaeassisted cathode by using C. vulgaris as biocatalyst in the suspension. The illumination periods and CO2 supply in the cathode chamber were studied to achieve maximum performance between 14 and 20 h of the cycle operation with higher polarization resistance at the cathode when compared to the anode. During the acclimation stage, power density increased up to 13.5 mW/m2 at steady state conditions. This mediator-less system illustrated CO2 fixation in the cathode chamber, while the wastewater (synthetic fruit processing industry effluent) was treated in the anode chamber. Gonzalez et al. [109] evaluated the biofilm formation of algae on cathode electrode and its effect on the performance of PMFC. This biofilm formation showed positive effect, depicting the decrement in cathodic polarization resistance thereby facilitating reduction reaction for enhanced bioelectricity generation [109]. The cathodic and anodic half cells consisting of photosynthetic microalgae, C. vulgaris, and fermentative yeast, respectively, were integrated to form a coupled MFC [110,111]. C. vulgaris is a commonly used microalgal species in the cathodic chamber of PMFC due to its versatile growth and ability to uptake CO2 and nutrients at a faster rate. Photosynthetic biocathodes using microalgae C. vulgaris to generate O2 by reducing atmospheric CO2 were investigated in the presence of mediator compounds by Powell et al. [111], by varying different parameters (CO2 concentrations, pH, radiant flux, mediator concentrations etc.). The C. vulgaris utilized 10% CO2 as the carbon source and showed power density of 2.7 mW/m2 of the electrode surface, cell growth rate of 3.6 mg/L h at high radiant flux condition (32.3 mW). This study has claimed that the mediated electron transfer played a significant role in transferring the electron from the cathode to the O2 produced by photosynthetic microalgae. The presence of mediators showed limited algal growth due to the attributed reduction in illumination caused by the mediator (methylene blue).

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Apart from utilizing the atmospheric air as source of CO2, studies were also performed on carbon and nutrients uptake from wastewater. Venkata Mohan et al. [48], studied the synergistic association between bacterial fermentation and oxygenic photosynthesis of mixed microalgae at anode and cathode chambers, respectively, in dual-chambered MFCs. The experiments were conducted to evaluate the power generation along with wastewater (domestic wastewater) treatment in two seasons, spring and summer. The results depicted higher bioelectrogenic activity (57.0 mW/m2) in spring in comparison with summer (1.1 mW/m2) due to the higher DO levels by oxygenic photosynthetic activity of microalgae. Similarly, landfill leachate was used as carbon source for microalgae present in the cathode chamber thereby treating the wastewater (carbon: 52%; NH4: 98.7%; phosphorus: 80.28%) and generation of 300 mV in a dual-chambered MFC configuration [86]. Flue gas from various industries contains large amounts of CO2 and NOx (source of nitrate), which acts as a suitable buffering agent and potential electron acceptor, respectively [112]. In this the microalgae utilize the exhaust gas (CO2) from different industries and light to generate biomass, which in turn used for biofuel generation, extraction of value-added products, and it can also be used as a biofertilizer [4]. 3.7.2.3.2 Integrative Process (Dual Chambered) In comparison with conventional MFCs, algae-assisted MFCs represent more advanced technique as they are capable of fixing CO2 with simultaneous wastewater treatment and bioenergy generation. For the cathode compartment to maintain high-energy generation, CO2 gas should be continuously sparged, and this remains an unsustainable way in terms of the economy during PMFC operation. Apart from industrial emissions, microalgae utilize the CO2 obtained from bacterial metabolism and respiration. Hence, the new concept of microbial carbon capture (MCC) was demonstrated as integrative configuration by Wang et al. [113], in which the CO2 gas generated in the anode chamber of MFC is introduced into the cathode chamber for its conversion to O2 via algal photosynthesis. The effective technology of MCC aids in the elimination of CO2 emissions and power consumption without the need for mechanical aeration. This CO2 introduction in the algal biocathodes helps in maintaining catholyte pH, alkalinity, and conductivity. Wang et al. [113] developed a PMFC termed as MCC that used microalgae C. vulgaris to form biomass by reducing CO2 emissions obtained by metabolism of 1 g/L glucose in the anode. This MCC depicted the comparable voltage output of 610 mV to corresponding MFC mode operation (630 mV) thereby demonstrating the utilization of anodic off gas as source of carbon to microalgae present in the cathode chamber of MCC. This showed the possibility of novel methods for simultaneous carbon fixing, power generation, treatment of nutrient rich wastewater, biomass growth, and less energy consumption. Though algae in biocathode are capable of generating enough O2 required for completing the cathodic reaction, the fluctuations in DO concentrations and bioelectricity generations have led to increase in cathode polarization resistance. To overcome this resistance, the immobilized C. vulgaris was used in the cathode of MCC to fulfill the zero discharge of CO2. Immobilized configuration showed higher chemical oxygen demand (COD) removal, power density, and columbic efficiency [114]. Liu et al. [115] also demonstrated the maintenance of photosynthetic algal biocathode by self-capturing CO2 released from the anode and utilizing solar energy as the energy input. Under the influence of light illumination and anodic off gas, PMFC generated 187 mW/m2 power density, which is far higher

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compared to dark conditions. This study also shows the occurrence of algal photosynthesis for the O2 generation by CO2 crossover from an anode to the cathode through the Nafion membrane, providing further understanding and improvement of algae-based MCC. By utilizing dead algal biomass as carbon source at anode chamber and CO2 (generated in anode) and sunlight at cathode chamber, the PMFC was compared with acetate-fed MFC by generating maximum power density of 1926 mW/m2. The harvested biomass at cathode can be used for extracting oil, and the residual biomass can be utilized as anode substrate thereby recycling the process and achieving economic viability [116]. Due to limited research conducted, the technology of MCC is still in its infant stage and requires further research to commercialize the process. In another integrative concept, algal photo bioreactors are connected in integration to either anode or cathode of MFC for continuous operation depending on the objective of the study. This integrated cells aid in recirculation of nutrients and CO2 produced for their utilization. The photosynthetic algal microbial fuel cell (PAMFC) study conducted by Strik et al. [117], describes the proof of principle based on naturally selected electrochemically active microorganisms and algae without adding any mediators in an open system. In this study an autotrophically operated algal photobioreactor (bubble column) was connected to the anode chamber of flat plate MFC and recirculated using peristaltic pumps. This study also suggested the development of low energy input PAMFCs as current algae production systems have energy inputs similar to the energy present in the out coming valuable products. This type of integrated MFC is easy to operate and cost effective as it operates in the absence of ion exchange membranes. Similar work of integrating an algal bioreactor to cathode chamber of an MFC in order to increase the availability of high O2 concentrations thereby enhancing the overall power generation was studied by Kakarla et al., [31]. This integrated MFC showed the increase in power density by 30% when compared with atmospheric air operation. Whereas, Hu et al. [118], evaluated the air-lift-type microbial carbon capture cell (ALMCC) by using an air-lift-type photo bioreactor as the cathode chamber for the first time, and the anodic effluent was integrated to the cathode chamber for further treatment by microalgae. ALMCC system designed with the inherent advantages of both MCC cell and air-lift-type photobioreactor that were studied by Wang et al. [113], and Ranjbar et al. [119], respectively, produced a maximum power density of 972.5 mW/m3 and removed 69% of phosphorus, 71% of ammonium nitrogen and 87% of COD. Besides this, ALMCC also demonstrated higher lipid productivity and CO2 fixation rate suggesting the net energy of the ALMCC was significantly superior to control systems [108]. The schematic of ALMCC has been illustrated in the Fig. 1 of Hu et al., [118]. And in extension of this work, Hu et al. [84], evaluated the ALMCC for different cathodic microorganisms (C. vulgaris and Chlorella sp.) under different light intensities. The ALMCC system with C. vulgaris depicted higher lipid productivity of 21.75 mg/L d, CO2 fixation rate of 223.68 mg/L d, and power density of 558.22 mW/m3 at 8.9 W/m2 optimal light intensity depicting the influence of light intensity on the operation of microalgae in biocathodes. Similar studies were reported to provide more economical alternatives to conventional tertiary treatment processes for nutrient removal [88]. 3.7.2.3.3 Three-Chambered Desalination Cell Apart from dual-chambered MFCs, algae are used as photosynthetic organisms in threechambered microbial desalination cells (MDCs). In this study the algae cathode

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3.7.2 ALGAL BIOCATHODES

537

(C. vulgaris) was comparatively evaluated with air cathode under passive conditions. The results suggested the enhanced performance of algal biocathode in terms of COD removal, nutrients utilization from wastewater toward biomass generation, maximum power density (151 mW/m3), and desalination rate (40%) when compared to air cathode. The algal biocathode showed desalination rate of 0.161 g/l/d, which is about 2.1 times higher than the corresponding air cathode operation (0.076 g/l/d). The higher potential difference between electrodes might be the probable reason to stimulate the ions transfer from middle chamber to anode and cathode based on charge. This study of cathode-driven processes provides an environmentally benign approach, in which algae can serve as an in situ O2 generator suggesting further developments in the MDC reactor design and electrode/material configurations for enhanced performance via. an environmentally sustainable manner [120]. 3.7.2.3.4 Photosynthetic Sediment MFC Sediment MFC is a type of MFC in which the anode is buried in the sediment, while the cathode is placed on top of the sediment. This configuration is also referred to as benthic MFC. The biocatalyst present in the sediment oxidizes the organic material while the cathodic reactions include reduction of atmospheric air (O2). The naturally existing differences in electropotential of the anode and cathode help in generating bioelectricity [121]. Jeon et al. [122], proposed a new approach of photosynthetic sediment MFC (PSMFC) which incorporates the microalgae in the cathode compartment. In this study the anode and cathode chambers were filled with sediments and photosynthetic microalgae, respectively, and are separated by a sand layer. The CO2 produced by anodic bacterial activity is consumed by algal cells, and the O2 produced by the algae is consumed by the PSMFC cathode compartment for current production. In another study the photosynthetic biocathode was covered in a biofilm composed of a complex community, including microalgae and cyanobacteria. This bioreactor is operated in the absence of proton exchange membrane and suspended photosynthetic oganisms in the cathode. The photosynthetic biofilm produced approximately four times higher DO levels than the aerated cathode, and the MFC was able to generate a maximum power density of 11 mW/m2 over 6 months without feeding. Table 3.7.1 provides the information about different types of MFC operation with algal biocathodes and other parameters that influenced the power generation.

3.7.2.4 Factors Influencing MFC Performance With Algal Biocathodes The PMFC operation is influenced by many parameters viz., biocatalyst type, mode of nutrition and operation, organic carbon, nitrogen, phosphorus and potassium (CNPK) ratios, CO2 concentrations, bioreactor configuration and operation time, membrane, light intensity, electrode size, material and distance, illumination, poised potential application etc. [89]. However, a detailed investigation on PMFC parameter optimization is limited in the literature due to the upcoming area of research. Various algal organisms, viz., marine/freshwater algae, micro/macroalgae, pure/mixed culture etc., have been investigated by many researchers to fit into respective objective of their work. During initial studies, marine algae were used as an O2 generator [45,85], while many freshwater algae have been utilized to study the bioelectricity and wastewater treatment in PMFC [84]. In a recent study

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538

3.7. ALGAL BIOCATHODES

TABLE 3.7.1

List of Different Algae Used in Microbial Fuel Cells and Maximum Power Generation

S. No Biocatalyst

Pure/Mixed

Bioreactor Configuration

Electrode Material

Power Generation

References

1

Chlorella vulgaris

Pure culture

Dual chambered

Glassy graphite rods

70 mV; 2.7 mW/m2 (Rext ¼ 0 U)

[111]

2

C. vulgaris

Pure culture

Dual chambered

Toray carbon cloths with 10% Teflon

18 mV (Rext ¼ 120 U)

[81]

3

C. vulgaris

Pure culture

Dual chambered

Toray carbon cloths with 10% Teflon

9 mV (Rext ¼ 120 U)

[109]

4

Mixed culture Mixed of oxygenic consortia of phototrophs specific pure strains

Dual chambered

Carbon fiber veil

169 mV (Rext ¼ 7.5 KU)

[108]

5

C. vulgaris

Pure culture

Dual chambered

Carbon fiber cloth (cathode) containing 0.1 mg/cm2 Pt catalyst

2485.35 mW/m3

[114]

6

Anabaena

Pure culture

Dual chambered

Noncatalyzed graphite

100.1 mW/m2

[112]

7

C. vulgaris

Pure culture

Dual chambered

Carbon felt containing 0.1 mg/cm2 Pt catalyst

187 mW/m2

[115]

8

C. vulgaris

Pure culture

Dualchambered ALMCC

Carbon fiber cloth

972.5 mW/m3

[118]

9

C. vulgaris and Chlorella sp.

Pure culture

Dualchambered ALMCC

Carbon fiber cloth

558.22 mW/m3

[84]

10

C. vulgaris

Pure culture

Dual chambered

Carbon fiber brush and carbon cloth

8.67 W/m3

[116]

11

Naturally selected microbes

Mixed culture

Photosynthetic Graphite felt algal microbial fuel cell (PAMFC)

110 mW/m2

[117]

12

C. vulgaris

Pure culture

Threechambered microbial desalination cells

Graphite papers

151 mW/m3

[120]

13

Microalgae

Mixed culture

Dual chambered

Carbon fiber brush and carbon cloth coated with Pt

0.63 W/m2

[31]

14

Mixed culture of green alga and iron-reducing bacterium

Chlamydomonas Single reinhardtii and chambered Geobacter sulfurreducens

Current density 0.2 mg platinum cm2, 4 polytetrafluoroethylene of 40 mA/m2 layers

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[83]

539

3.7.2 ALGAL BIOCATHODES

TABLE 3.7.1

List of Different Algae Used in Microbial Fuel Cells and Maximum Power Generationdcont'd Bioreactor Configuration

Electrode Material

Power Generation

Mixed Culture

Dual chambered

Graphite plates

Spring 57.0 mW/m2; Summer 1.1 mW/m2

[48]

C. vulgaris

Pure culture

Dual chambered

Anodes-carbon fiber brushes; Cathodescarbon cloth containing 0.1 mg/cm2 Pt catalyst on one side

5.6 W/m3

[113]

17

C. vulgaris

Pure culture

Sediment MFC Graphite Felt

33 mA/m2

[122]

18

Microalgae

Mixed culture

Dual chambered

Carbon fiber veil

128 mW

[88]

19

Microalgae

Mixed culture

Dual chambered

Carbon fiber brush and carbon felt

187 mW/m2

[115]

20

Microalgae

Mixed culture

Dual chambered

Plain carbon paper and 30 mW/m2 Carbon fiber brush/plain carbon paper

[51]

21

Microalgae

Mixed culture

Dual chambered

Carbon fiber brush

[86]

S. No Biocatalyst

Pure/Mixed

15

Microalgae

16

300 mV

References

Velasquez-Orta et al. [80], have provided comprehensive details related to the electricity production from both microalgae (C. vulgaris) and macroalgae (Ulva lactuca) in MFCs. Regarding pure and mixed culture operation of algae in PMFCs, numerous studies viz., different bioreactor configurations, substrates, source of biocatalyst, syntrophic interactions between electricity-generating bacteria and microalgal phototrophs etc. have been explored [81e83]. The next important parameter after biocatalyst is light intensity as it has a significant influence on the performance of the biocatalyst. Gouveia et al. [123], have investigated the influence of two different light intensities (26 and 96 mE/(m2 s) with results showing the maximum power of 62.7 mW/m2 at the higher light intensity. Similarly, influence of different light intensities (0, 1500, 2000, 2500, 3000, and 3500 lx) on Desmodesmus sp. A8 assisted biocathodes, in which the anode and cathode resistances were greatly reduced when the higher light intensity was used [124]. Moreover, many researchers have investigated the influence of different light intensities, illuminated and nonilluminated cycles etc., on performance of PMFCs [24,113,121,125e128]. However, the detailed report on the influence of bioreactor configuration on the performance of algae-assisted biocathode PMFCs is given in Section 3.7.2.3. Kakarla and Min

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3.7. ALGAL BIOCATHODES

[51], evaluated the influence of different cathode materials (carbon fiber brush and plain carbon paper) on the activity of PMFC performance utilizing Scenedesmus obliquus as the biocatalyst. This study also proved the benefit of algal O2 supply when compared with mechanical aeration in carrying out biocathode reactions. Many studies depicted the efficiency of sparging CO2 either from atmosphere [111,115] or from the anode chamber [112,113] for its efficient conversion and generation of O2 in the cathode chamber depicting the ability of autotrophic mode of nutrition by algae in biocathode. Gonzalez del Campo et al. [81], investigated the mode of operation optimization and showed that continuous operation achieved higher power output over sequencing batch mode operation. In rice-paddy MFCs the factors viz., anode position, cathode modification with Pt catalysts, and external load largely affected the overall power output [129].

3.7.2.5 Limitations of Algal Biocathodes MFC The algal biocathodes have the advantages of inferior costs, high-value biomass production through CO2 sequestration, minimal operational conditions, resistant to hazardous materials, high reaction rate etc., making the PMFCs an efficient and sustainable process. In spite of all these benefits they still have several limitations when compared with abiotic cathodes that need further improvement for practical applications [112,130]. General limitations include shortening of start-up time for biocathodes; slow activity of autotrophic mode of nutrition when compared with heterotrophic mode thereby affecting the MFC operation; energy losses due to occurrence of high over potentials; charge transfer resistance when operated in open air cathode; expensive when buffer systems are used as the algal biocathodes are sensitive to change in influent characteristics such as pH; lower performance of biologically catalyzed cathodes in terms of power generation when compared with chemically catalyzed ones; necessity for new PMFC configurations in order to adjust the supply of nutrients, CO2, and sunlight; reduction in biocatalyst activity when mediator solutions are used as the sunlight does not penetrate for algae to carry out photosynthesis mechanism; inhibition of photosynthetic activity due to blockage of relevant enzymes active site by adsorption of polyvalent cations on the algae cell surface, etc. that challenge the effective application of this technology [131,132]. In large-scale operations, microalgal MFCs with high-density biomass require a continuous and effective supply of CO2 and effective algal harvesting techniques, which makes it difficult for immediate practical applications [133]. The long-term operation of PMFC results in voltage drop due to alkaline microenvironment in the cathode chamber, increase in thickness of cathodic biofilm on a current collector, and a significant negative influence of the electrode on power generation. The crossover of organic materials from the anode to the cathode (electroosmosis and molecular diffusion) through the separating membrane will reduce the cathode potential, have a toxic effect on the photosynthetic organisms, and convert photosynthetic biocathode to irreversible anaerobic heterotrophic biofilm due to the inflow of high COD content and restricted O2 supply [50,87]. All these limitations act as bottlenecks for making PMFC a practical and commercial technology to replace abiotic cathodes.

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REFERENCES

541

3.7.3 CONCLUSIONS AND PERSPECTIVES MFCs with algal biocathodes are novel, renewable, promising, cost-effective, inorganic carbon fixer, and sustainable bioelectricity generation systems that further requires additional research and development on the aspects such as reducing the energy input, mass transfer limitation, and enhancing the photosynthetic efficiency of biocatalyst and thereby bioelectricity generation at commercial scale. The concept of integrating photosynthesis via biocathodes in which algae is used to drive the cathodic reactions came into existence as part of designing an MFC with high net energy production and low reaction losses. Optimization of various parameters and fundamental understanding of critical factors (conditions) that limits bioelectrogenic performance helps to overcome some of the inherent limitations of algal biocathode systems. Various conditions such as hydrologic regimes, substrate loading, influent pH, amount of DO, dynamics of microbial communities, poising potentials etc. were optimized to enhance the overall performance of algal biocathode MFCs. Algal electron transfer mechanisms in association with other pollutants should be fully evaluated. Study of electron transfer mechanism by both bacteria and microalgae helps in identifying the intermediates formed during the process, understand the reactions occurring at electron level, and regulate the degradation process as a whole. The syntrophic interaction of bacteria, cyanobacteria, and microalgae can serve as possible, promising, and advantageous alternative to algal biocathodes under batch and continuous mode of operations to make the overall process viable. Characterization of microorganisms in respective bioreactors will aid in identification and isolation of potential in situ oxygenators that aid in adopting bioaugmentation strategy. To elucidate the process as economically viable and environmentally benign, the PMFCs should be scaled up for a successful application. The operation of scalable MFCs having photosynthetic biocathodes should be incorporated with wastewater treatment facilities thereby exploring the possibility to power facilities for treatment (aerator etc.). Evaluation of different downstream processes for product recovery is the other possible potential areas for future research. Cost cutting research with an interdisciplinary approach will help to resolve some of the inherent limitations prior to scale up operation.

Acknowledgments The study was carried out with research grants from the National Research Foundation of Korea (2015R1D1A1A09059935) and Korea-India S & T Cooperation Program (2016K1A3A1A19945953).

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