Sustainable power generation from bacterio-algal microbial fuel cells (MFCs): An overview

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

Contents lists available at ScienceDirect

Renewable and Sustainable Energy Reviews journal homepage: www.elsevier.com/locate/rser

Sustainable power generation from bacterio-algal microbial fuel cells (MFCs): An overview

MARK

⁎

Beenish Sabaa,b, , Ann D. Christya, Zhongtang Yuc, Anne C. Cod a

Department of Food Agricultural and Biological Engineering, The Ohio State University, 590 Woody Hayes Drive, Columbus, OH 43210, USA Department of Environmental Sciences, PMAS Arid Agriculture University, Rawalpindi 46300, Pakistan c Department of Animal Sciences, The Ohio State University, 2029 Fyffe Road, Columbus, OH 43210, USA d Department of Chemistry and Biochemistry, The Ohio State University, 100 West 18th Avenue, Columbus, OH 43210, USA b

A R T I C L E I N F O

A BS T RAC T

Keywords: Bacteria Algae Microbial fuel cells Operational and electrical parameters

Microbial fuel cells (MFCs) are bioelectrochemical devices that allow the harvesting of electricity generated during anaerobic respiration of selected bacterial species. This technology shows promise in both wastewater treatment and sustainable bioenergy conversion applications. Bacterial respiration occurs in the anaerobic anode compartment of the MFC, and is electrochemically coupled with electron acceptors in the MFC's aerobic cathode compartment. This paper summarizes the published results of bacterio-algal MFCs. The use of microalgae in MFCs has gained interest primarily due to algae's ability to photosynthesize atmospheric CO2, producing both biomass and oxygen and thereby facilitating the cathodic reaction. These phototrophic microorganisms can serve as biocatholytes in MFCs because the oxygen produced is an electron acceptor for the electrons harvested from the anode compartment. The bacterio-algal MFC can provide multiple benefits including 1) power generation, 2) wastewater treatment, 3) algal biomass cultivation and pigment production, 4) carbon dioxide assimilation, and 5) oxygen production. This review article summarizes not only successful published results of bacterio-algal fuel cells but also highlights critical operational parameters and their effect on power generation and output efficiency.

1. Introduction Among newly developed renewable energy production technologies, the microbial fuel cell (MFC) is a promising technique because of its sustainability to directly convert waste into electrical energy [1–4]. MFCs typically consist of two compartments separated by a proton exchange membrane with an external circuit connecting anode and cathode electrodes. They can be categorized on the basis of catholyte; 1) abiotic catholyte e.g potassium ferricyanide, nutrient medium etc. 2) biotic catholyte e.g. algae, cyanobacteria etc. The second category hereafter is referred as bacterio-algal MFCs and will be the main focus of the present review. The bacterio-algal MFC is an approach to enhance the economic and carbon capture characteristics of MFC technology [5]. In this approach, autotrophic and phototrophic microorganisms are employed as a catholyte along with anode-reducing exoelectrogenic bacteria as an anolyte [5]. Algae can be introduced to either the anodic or the cathodic compartments of the MFC to serve as a source of carbon (substrate) or to generate oxygen, respectively. It can be cultivated within the cathode chamber by passively capturing CO2 from the atmosphere [7] or artificially sparging more concentrated ⁎

CO2 streams into the cathode chamber [8]. The required Sunlight can be provided naturally or by grow lights under laboratory conditions. Carbon substrate can be obtained by a variety of media such as glucose, formate, acetate and dry algae biomass. Direct use of the dry algae as a substrate is problematic because it is difficult for bacteria to hydrolyse algal cell walls [9]. Glucose, formate and acetate substrates are simple sources of carbon which are readily available to bacteria, but they are more expensive [5,10] as compared to the waste sources such as domestic wastewater [10], activated sludge [11], landfill leachate [12], food processing leachate [13], and other waste materials. The utilization of wastewater as a substrate in bacterio-algal MFCs for power generation is widely studied inexpensive nutrient source in laboratory experiments [9,14,15]. Different configurations of bacterioalgal MFCs with various electrode materials [13,15,16], variety of substrates and microbial sources have been employed [6,8]. Some of these techniques have promising results [2,4,9,17] but the environmental and economic life cycle assessment of these systems is needed for their practical application. In this current review we aim to summarise the published research on the performance of bacterioalgal MFCs and their limitations for the commercial applicability.

Corresponding author at: Department of Food Agricultural and Biological Engineering, The Ohio State University, 590 Woody Hayes Drive, Columbus, OH 43210, USA. E-mail address: [email protected] (B. Saba).

http://dx.doi.org/10.1016/j.rser.2017.01.115 Received 4 May 2016; Received in revised form 25 November 2016; Accepted 17 January 2017 1364-0321/ © 2017 Elsevier Ltd. All rights reserved.

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

2. Bacterio-algal fuel cell technology 2.1. Algae as biocatholyte Photosynthesis is one of the most complex biological redox reactions. In this reaction, natural solar energy and carbon dioxide are the inputs to a process that produces carbohydrates, oxygen and additional compounds including proteins, pigments, and oils. Autotrophic growth of algae can be supported in artificial environments. Photobioreactors [18], algal ponds, and lagoons [19] are some of the common techniques used to grow and harvest algal biomass. Heterotrophic growth of algae in the dark, supported by consumption of various carbon substrates, is a unique ability of microalgae [20]. However, this heterotrophic mode of algal growth can be subject to contamination and growth competition from other microorganisms [20]. In photobioreactors, algae cultivation is operated in mixotrophic mode (i.e., autotrophic+heterotrophic). This mixotrophic property of algae makes it a suitable candidate as an MFC biocatholyte, along with its other abilities such as oxygen production and CO2 assimilation, and its logarithmic growth pattern [21]. Bacterio-algal MFCs are operated on the premise that substrate is oxidized by bacteria in the anolyte and oxygen is produced by the algae in the catholyte. This oxygen acts as an electron acceptor, reducing CO2 and producing water and more algal biomass via photosynthesis [22–24] (Fig. 1). The chemical equations for photosynthetic reactions in the cathodic chamber of algal-MFCs are as follows: Light reaction

Fig. 2. Schematic presentation of algae-electrode interaction.

important role in the performance of the electrochemical system [28]. Biofilm formation on the cathode acts as a direct mediator in electron transfer and reduces ohmic and charge transfer resistance losses in the MFC [29,30] (Fig. 2). 2.2. Bacterio-algal fuel cell configurations Three major configurations of MFCs are currently in use for simultaneous growth of bacteria and algae: (1) single chamber MFCs, (2) two chambered MFCs, and (3) three chambered MFCs. Schematics of different configurations of MFCs are shown in Fig. 3. Each of these designs is described more fully below. Single chamber bacterial-algal MFCs (Fig. 3A), in which bacteria and algae are grown together in one chamber, are usually configured with an air cathode [17,31,32]. Single chamber MFCs are membraneless, easy to operate, and cost effective in scaling up. Autotrophic and heterotrophic microorganisms are grown simultaneously so 100% consumption by algae of the CO2 generated by the bacteria is possible. In single chamber MFCs, bacterial co-cultures can grow synergistically with algal co-cultures [17]. Single chambers are easy to manage in lab as compare to other configurations. In two chambered MFCs (Fig. 3B), algae and bacteria exist in separate chambers which are connected by a cation exchange membrane [9,33]. In two chambered MFCs, a light source is usually placed on algae side. This serves to provide photons for the algal photosynthetic reactions in the cathodic chamber but also illuminates the bacterial compartment, leading other researchers to cover their anodic chambers during experiments [10]. In some studies, an external algae photobioreactor (Fig. 3C) provides the MFC with a continuous supply of algae [10,34]. Membrane crossover and relatively high internal resistance are some of the problems associated with dual chamber MFCs. Photobioreactors provide a continuous source of algae which is easier to maintain, but the addition of pumping reduces net power generation. H-shaped (Fig. 3D) two chambered MFCs have also been used in earlier studies with the disadvantage that the membrane area between the anolyte and catholyte is very small. Ion exchange between two chambers is very low, in turn producing low power output. Membrane fouling and internal resistance can effect efficiency of two chambered MFCs. In three chambered MFCs, an additional middle chamber containing salt water is also present. Cations move towards the cathode, anions move towards the anode, and partial desalination is observed in the process (Fig. 3E). The presence of salt water in the middle chamber can pose a stress on power production and its peak power density has been observed to be lower than two chambered MFCs [35,36]. Other configurations of MFCs include a tube shaped MFC which is a kind of single chamber MFC [31] and a lagoon or algal pond MFC in which anodic chambers are submerged in a bath of algae within a larger lagoon. Power production and biomass content can be optimized according to local weather conditions in any configuration.

6CO2+12H++12e-→C6H12O6 (biomass)+3O2 Dark reaction C6H12O6 (biomass)+6O2→6CO2+6H2O Cathodic reaction O2+4H++4e- →2H2O Algal growth in the cathodic chamber is a self sustaining cycle. Over time, algae growing in suspension can form a biofilm on the electrode and chamber surface. Algal biofilm directly accepts electrons traversing the MFC circuit and these electrons penetrate into the algal cell body [25]. For planktonic algal suspensions, intermediate mediators are used which can accept electrons from the cathode and deliver them to the suspended algae. These reduced mediators penetrate algal cells, deliver their electrons thereby becoming oxidized, and then are released from the algal cells back into the catholyte [26,27]. Dissolved oxygen within the algal biofilm has been verified to play an

Fig. 1. Concept of mixotrophic biological reactions in algae.

76

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

Fig. 3. Bacterio-algal microbial fuel cell configurations (A) single chamber (B) Dual chamber (C) dual chamber with photobioreactor (D) three chamber with desalination (E) H type dual chamber.

membrane type and internal resistance are the factors effecting power generation. Columbic efficiency and power production depends on number of factors like resistance of membrane, high ion generation in anodic chamber, oxygen cross over through membrane or membrane is highly porous. Therefore low resistance and high conductivity and non porous, highly selective membranes should be employed. Membrane fouling, high COD and low pH are some other factors which can lower membrane efficiency [41]. To solve these problems, membrane pretreatment and continuous monitoring of the anodic chamber’s internal conditions are necessary. Cation proton exchange membranes are used in MFCs depending upon reaction kinetics. Single chamber MFCs are membrane-less, which avoids membrane losses but can cause oxygen to more easily cross into the anaerobic anode chamber. Depending on the type of micro-organisms present in the anolyte, this can cause facultative anaerobes to switch metabolic pathways away from electricity generating anaerobic respiration, can be deadly to obligate anaerobes, and can cause changes in microbial consortia for mixed cultures. For example, aerobic microorganisms present in wastewater sludge can outcompete anaerobic microbes leading to lower power production. Table 1 summarizes the type of membranes used in dual chamber bacterio-algal MFCs.

2.3. Types of innocula in bacterio-algal MFCs Common sources of innocula for MFC anodic chambers include pure microbial cultures, defined microbial consortia, and undefined microbial consortia such as municipal wastewater, anaerobic bioreactor effluent, anaerobic sludge [15,31,33]. Synthetic wastewater [37] and rumen micro-organisms [38] have also been used. Rumen microorganisms have added benefits such as faster acclimatization as compared to municipal wastewater microorganisms and the ability to hydrolyse cellulosic biomass substrates. Leachate from landfills and food waste has also been successfully used [39]. Some single specie inoculation in the anodic chamber have been used including Geobacter sulferreducens [17], and Shewanella oneidensis [40]. Biofilm and suspended planktonic analysis of the microbial community in the anode chamber of a MFC inoculated with activated sludge showed Desulfovibrio sp., P. aeruginosa, Cytophaga xylanolytica, Dechloromonas sp., Thiomonas perometabolis, and Cytophaga sp. as dominant species [9]. The source of innocula in the cathodic chamber of bacterio-algal MFCs is algae. Algae are introduced to MFCs to increase the oxygen concentration in the catholyte and to absorb CO2 either from ambient air or diverted from the anodic chamber. Chlorella vulgaris [6,14,18] is a common cathodic algae. Other species of Chlorella [40], marine algae [33], blue green algae and cyanobacteria [31] have also proven their usefulness in bacterio-algal MFCs. Table 1 summarizes algae used in bacterio-algal MFCs as documented in the research literature. A variety of algal species including pure culture, co-cultures, and mixed cultures have been employed.

2.5. Catholytes in bacterio-algal MFCs The major difference between common MFCs and bacterio-algal MFCs is the presence of algae in cathodic chamber. Algae oxygenates the cathodic chamber and yields additional algal biomass and pigments. Oxygen generated by algal photosynthesis accepts electrons at the cathode. Algae is tolerant of changes in cation concentrations due to other ions crossing the membrane from the anode chamber. Algal biomass produced can be used as a valuable by-product either as a source of animal feed or for energy and bioproduct generation via anaerobic digestion [42] or other bioprocess. Biomass production in batch reactions with higher hydraulic retention times (HRT) produces more algae than a continuous system with lower HRTs. By circulating algal biomass between a separate photobioreactor and the MFC’s cathodic chamber [34], this disadvantage of continuous operation can be overcome.

2.4. Anolytes in bacterio-algal MFCs Electricity production and COD removal characteristics of MFCs depend primarily on the redox reactions in the anode chamber. Different carbon sources have been studied for use in the anolytes of bacterio-algal MFCs. Most common are glucose [14], formate and acetae [17]. Other prepared sources include LB medium [40], GSMM [33], Scenedesmus algae in powder form [8], GM medium [29], fruit industry liquid waste [23], and synthetic wastewater [37]. MFC 77

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

Table 1 Power density of Bacterio-algal MFCs.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

Cathodic contents

Anodic contents

Power output (mW/m2)

References

Blue green algae Chlorella vulgaris Scenedismus obliquus Desmodesmus sp. Chlorella and blue green Phormidium Chlorella vulgaris Mix algal culture Laminaria saccharina liquor (autoclaved) Laminaria saccharina liquor (Microwaved) Chlamydomonas reinhardtii Chlamydomonas reinhardtii Chlamydomonas reinhardtii Mix algae Spirulina platensis Scenedismus obliquus Chlorella vulgaris Chlorella vulgaris Chlorella vulgaris Mixed algal culture Synechococcus leopoliensis, Anabaena cylindrical, Chlorella pyrenoidosa

Anaerobic wastewater sludge Activated sludge GM media only Synthetic wastewater wastewater Enriched bacterial consortium Municipal wastewater Wastewater microbial consortium Wastewater microbial consortium

114 13.5 153 99 263 62.7 11.5 218 118

[31] [11] [29] [37] [10] [16] [15] [33] [33]

Geobacter sulferreducens Geobacter sulferreducens +Acetate Geobacter sulferreducens +Formate Activated anaerobic sludge – Activated sludge Scenedesmus enriched anaerobic activated sludge Domestic wastewater – Anerobic suspension from growth reactor Shewanella oneidensis

41 630 140 – 10 1.78 W/m2 514 5.2 W/m3 48 mA/m2 57 0.0033

[17] [17] [17] [34] [25] [9] [18] [14] [6] [17] [40]

successful growth of Chlorella vulgaris. The different varieties of algal species across all of these studies required different growth media and exhibited different growth parameters which in turn caused variation in power production.

Table 2 COD removal efficiency of bacterio-algal MFCs. S.No.

COD removal (%)

References

1 2 3 4 5 6

81 80 80 90 88 74% in cathodic chamber and 37% in anodic chamber during spring 58% in cathodic chamber and 27% in anodic chamber during summer

[10] [31] [11] [18] [33] [48]

7

2.6. Electrode materials Different electrode materials have been studied for use in bacterioalgal MFCs. In search of improved electrode performance, researchers have studied a variety of materials, surface geometry area enhancements, and surface modifications. Carbon based electrodes are used due to their chemical stability, electrical conductivity, low cost, and support of bacterial adhesion to form stable biofilms. Commonly used materials are graphite plates and rods, carbon fiber brushes, carbon cloth, carbon paper, carbon felt, carbon nanotubes, and granulated graphite. Among these, plain graphite and graphite felt are the most studied forms of cathodic material in bacterio-algal MFCs [17]. Various coatings have been explored including platinum and 10% Teflon and coated carbon paper has also been reported to support algal biofilm formation on the cathode. Table 3 summarizes the types of anodes and materials reported for use in bacterio-algal MFCs. Most of the studies used the same materials for both anode and cathode, but in some studies they have used different materials to increase surface area for biofilm formation on one or the other electrode [8]. Table 4 summarizes the use of different electrode materials in published studies, their drawbacks, and benefits. Materials for MFC chamber construction ranges from a variety of plastics to glass. Use of any specific material has not proven to have any effect on MFC power production. Most frequently, copper wire was used for electrode connections [13,29,54], but some researchers have used titanium wire [9]. The advantages of copper wire include its high thermal and electrical conductivities, and its mechanical characteristics of high tensile strength and ductility. The corrosion resistance of copper also makes it very suitable for use in liquid MFC systems [49]. However price of copper wires increases the capital cost of MFCs.

[48]

A limiting step in power generation is the rate of oxygen reduction to water in the cathode chamber. Oxygen reduction can be enhanced by applying a catalyst at the cathode [43] or by adding a strong reducing salt such as potassium ferricyanide [44] to the catholyte; other methods for increasing oxygen availability include sparging air or pure oxygen into the cathode chamber or by rotating the electrode [45]. However, algae cultivation within the cathode chamber can provide a more consistent and continuous source of oxygen [11]. Thick algal biofilms on the cathode surface can limit oxygen diffusion and MFC performance [46]. Algal biofilm growth and thickness depends on the electrode’s surface texture; highly porous and/or rough surfaces favour thick algae biofilm growth while smooth surfaces support thin biofilm growth which is the better option [16]. Monitoring algal growth by collecting optical density measurements in the cathode chamber is challenging given that the growth occurs in three forms: as algae biofilm on the electrode and chamber walls, as suspended algal aggregates, and as suspended biomass in solution. Algae biomass monitoring by weighing dry biomass samples or assaying for protein content are other feasible options. A wide variety of catholytes has been used in bacterio-algal MFCs including Bold's Basal Medium with 300 mg/dm3 algal biomass [6,11], a mixture of 1 g NH4Cl and 0.13 g of KH2PO4_H2O in tap water [10]. Gouveia et al. [47] produced 2800 mg/l of biomass using 50 mM PBS as the catholyte nutrient medium. Bold Basal Medium containing algae (0.93 g/l), sodium bicarbonate (NaHCO3, 2 g/l) as a carbon source, and 100 mM PBS was the catholyte composition reported by Kakarla and Min [29]. Mohan et al. [48] used domestic sewage as their catholyte with the addition of glucose and urea as carbon and nitrogen sources respectively, while Wang et al. [14] used 50 mM NBS with BG11 for

3. Operational parameters 3.1. Light intensities In the algal cathodic chamber both oxidation and reduction reactions occur when algae are provided 12 h light and 12 h dark 78

79

Graphite plates

Carbon fiber veil Single chamber Graphite carbon Carbon cloth

12

13

Graphite felt

18

17

Carbon paper Platinum coated Air cathode

16

14 15

Carbon cloth

Carbon fiber veil

8

11

Graphite felt

7

Carbon brush

Toray carbon cloth 10% Teflon

5

10

Plain graphite felt

4

Anode

Graphite felt

Plain carbon paper

Gliding gold mesh Graphite felt roll

Carbon cloth+Pt catalyst Carbon fiber brush

Carbon fiber brush

Graphite

3

Carbon cloth

Carbon cloth

2

9

Two chamber Graphite carbon

1

Cathode

PEM

–

Membrane less Membrane less Membraneless

– –

Membrane less Membrane less

CEM

PEM

CEM

CEM

Glass bottle

Glass PVC tube

Acrylic

Poly acrylate

Plexiglas

acrylic

CEM

CEM

– acrylic

–

–

PEM

CEM

PEM

–

Plexi-glass

PEM

Membrane

Acrylic

MFC material

Table 3 Types of electrodes and configuration of bacterio-algal MFCs.

2

81 µmol/m s

20 W/m2

5000 lumen

– –

30 W

–

25 W

–

2000 lux

–

–

11 W

3000 lux

96 µ E/m2S

6–12 W 12–18 W 11 W

Light intensity

Light to electricity conversion is result of syntrophy between phototrophs and autotrophs but oxygen production by phototrophs is negatively effecting anaerobic G.sulferreducense in single chamber Higher algal biomass can be obtained at lower resistance When wires are connected for current production CO2 generation increases and CH4 generation decreases.

89% COD removal, 96% NH4 removal along with > 90% microsystein (neurotoxins) removal was observed in this study Algae producing oxygen in electrode chamber produces 32% higher power output than mechanical aeration

Different light intensities were evaluated in MFC with algae growth and low light intensity is producing high power output is proved in this study. Light was provided in 12 h day night cycles, CO2 was bubbled through the system and lagooning microbial fuel cell was studied in this work. Pigment extraction and quantification was performed under normal and starved nitrogen conditions, Chlorophyll, lutein/zeuxathin, βcarotene and cathaxathine were among the main extracted pigments. Light intensity MFC output has a linear relationship of increase in illumination negatively effects cathodic resistance CO2 bubbling for 30 min is enough time to get system working and high polarization resistance in algal cathode was observed than anode. Algae liquor was added in anodic chamber as co-substrate for microbes and power production capacity was compared with glucose as carbon source They used algal photoreactor attached with cathodic chamber and catholyte was continuously circulated between chamber and photoreactor CO2 produced in anode is diverted cathodic chamber for algal growth and very reduced algae growth was observed when fed with acetate Pre-treated (sonicated) and lipid extracted algae produces less power as compare to non pre-treated and nonextracted algae. Open cathodic chamber are helpful in ambient CO2 sequestration with simultaneous voltage output without aeration. Chlorophyll content produced by algae is higher in spring while lower in summer while VFAs are higher in summer and lower in spring. Oxygenic phototrophic biofilms can enhance cathodic performance

Comments

[6]

[17]

[29]

[25] [31]

[40]

[48]

[14]

[9]

[37]

[34]

[33]

[11]

[37]

[16]

[15]

[10]

Reference

B. Saba et al.

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

Table 4 Listed are some types of electrode materials with advantages and drawbacks of materials used in MFCs. Electrode types

Benefits

Drawbacks

References

1

Graphite plate

Defined surface area, high conductivity, inexpensive

[83]

2 3 4 5

Graphite fiber brush Carbon cloth Carbon paper Carbon felt

High porosity 95–98% Large porosity Easy electrical connection Easy electrical connection

6 7

Carbon nanotubes Graphene modified

Very high surface area Better electrochemical performance, Anti-corrosive

Low surface area Good bio-compability Clogging, un-excess able sites for bacteria relatively expensive Non durable, high resistance, fragile High resistance, clogging Toxic to microbes Expensive, highly brittle

[84] [77], [85] [86] [86] [85], [87] [88]

concentration fluctuates diurnally and is also affected by temperature. During night time hours DO levels drop due to algal respiration and inhibition of photosynthetic activities, while in daylight hours it is raised as a product of photosynthesis. Jung et al. [10] observed that when temperature was raised from 27 to 31.2 °C, DO concentration in catholyte containing Chlorella vulgaris raised from 3.7 to 6.8 mg/L. In comparison, the solubility of oxygen in fresh water is reduced from 7.97 to 7.43 mg/L when temperature increases from 27 to 31 °C (Oxygen Solubility Table [updated 2016]). Temperature effects on DO in an algal enriched catholyte may be due to a combination of responses to changes in light intensity of the artificial lamp as well as ambient temperature variations. When the power of the artificial lamp is increased from 6 W to 26 W, the rate of photosynthesis and DO concentrations are both raised [10]. Temperature, DO, and rate of photosynthesis are all interdependent. Critical values of DO for maximum MFC power production ranges between 4.5 and 5.5 mg/L [10,58]. Wu et al. [37] observed 13.2 mg/L DO at higher illuminance (3500 lux) which increased photosynthesises and thus algal DO production. Supply of more light reduces the power production of MFC. As light levels increase, the resulting higher oxygen gradient between the MFC chambers also may drive oxygen to cross over from the cathodic chamber to anodic chamber. Too high of light intensity can actually slow down the photosynthetic process, called photo-inhibition [14]. Lobato et al. [15] observed that cathodic processes, and specifically DO concentrations, control the overall performance of the bacterio-algal MFC. For the two selected light intensities (26 µE/m2s and 96 µE/m2s) reported by Gouveia et al. [47], the higher light intensity resulted in 10xhigher growth rate of microalgae and 6 x higher power production, along with increases in oxygen concentrations and pigment production. Bio cathodes allows expensive noble catalysts employed for the oxygen reduction can be replaced by algal biocathodes [24,34].

cycles. During light period photosynthesis, algal biomass production and oxygen production (oxidation) occurs, and during the dark period algae consumes oxygen and oxidizes organic matter (reduction) previously produced. Algae produces 60% of light cycle electricity during dark cycle, and substances other than oxygen act as electron acceptors [11]. A recent study [37] suggested that higher light intensity and optimal dark and light cycles decreased cathodic resistance and increased power production, but Juang et al. [10] observed that light power had a inverse relationship with current density, voltage production and columbic efficiency. Juang et al. [10] applied two different sets of lights, one rated at 6–12 W and the other 12–18 W; higher power production was observed at the lower light power. Relatively higher power was observed when the anodic chamber was covered; one reason may be that some algae present in anodic chamber start growing in the presence of light and produces oxygen. The difference between power production with covered versus uncovered anodic chambers was 4.41 mW/Kg COD/day. Wu et al. [37] observed 1.5 times higher power production when light intensity was raised from 1500 lx to 3500 lx. The profound effect of increasing light intensity on power production is evident from these studies. 3.2. Carbon dioxide To promote algal growth, different media and nutrients were supplemented, along with sparging of CO2 for enhanced photosynthesis. Campo et al. [11] found that 30 min sparging of CO2 into the cathodic chamber produced optimal growth while Wang et al. [14] and Cui et al. [8] diverted CO2 produced by bacteria in the anodic chamber into the cathodic chamber; their studies suggested that continuous bubbling of CO2 was not required. Daytime electricity production strongly depends on organic loading rate and light irradiation. Myerse et al. [50] demonstrated that algal cells prefer to use CO2 in the presence of light and organic carbon. Cao et al. [51] observed inorganic carbon (IC) in the cathodic and anodic chamber and came to conclusion that algae fix CO2 by utilizing IC and additional bacterial CO2 emitted from anodic chamber which can also permeate through the membrane and be consumed by microalgae. Solubility of CO2 poses a negative effect on algae growth in early stages. CO2 interaction with water forms H2CO3 and lowers pH [52]. To overcome this pH problem, algal inoculation should be initially high [53]. CO2 concentration also affects the lipid content of microalgae. The cells produce poly-unsaturated fatty acids under high CO2 concentrations [54]. A 6% lipid content increase was observed accompanied by a 10–15% increase in CO2 supply [55]. Addition of carbon dioxide does not improve biodiesel quality however biomass production rate and quantity of biodiesel produces is effected positively [56].

4. Electrochemical parameters 4.1. Polarization curves Changing external loads lead to alterations in the power generation profile of the MFC. Polarization curves are usually plotted as power density (PD) and corresponding voltage versus current density under varying external resistances. The external load at which maximum power density is obtained during polarization testing is the cell design point (CDP). In most MFC research, the external resistance step test procedure which is used to generate polarization curves is applied when the system's performance is stable which produces a constant output over the cycles. Other bacterial-algal MFC researchers prefer to perform step tests with every light-dark cycle of the photosynthesis process resulting in the generation of several polarization curves; for example Chandra et al. [59] reported polarization curves for their bacterio-algal MFCs with 6 cycles of day and night performance. Their observations showed improvement in power density from 17 mW/m2

3.3. Dissolved oxygen Dissolved oxygen (DO) concentration in the catholyte is one of the most important parameters which control MFC performance [57]. DO 80

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

(cycle 1) to 72 mW/m2 (cycle 6). The reason is that over time the total biomass has increased, resulting in more electron transfer from biocatalyst to anode. Over progressive cycles, ohmic losses (due to losses from electrodes, electrolytes, and membranes) and activation losses (due to biomass growth and metabolism kinetics) were observed to decrease. Power output of an MFC can be maximized when external resistance is equal to internal resistance. Higher power production depends on internal resistances, and in a bacterio-algal MFCs internal resistance is not affected by changes in light intensity [60].

catholyte. Ohmic and polarization resistances decreased over time [29] which could be due to excretion of organic substances from growing algal cultures, such as amino acids, hormones and lipids [64] but more studies are needed. 5. Perspective benefits of bacterio-algal MFCs 5.1. Useful algal by-products Evaluation of the pigment content profile of algae is another way to validate alga growth and photosynthetic activity. Chlorophyll content reflects the photosynthetic activity of algae in the cathode chamber for simultaneous energy supply, oxygen release, and CO2 utilization. Mohan et al. [48] observed 0.8 g/L algal biomass growth in the spring and 0.9 g/L in the summer. Chlorophyll content increased from 7.21 lg/mg to 15.61 lg/mg with operating time. Seasonal changes in terms of temperature change affects algal growth and its associated photosynthetic activity. Elevated summer temperatures can result in suppressed chlorophyll content. Higher temperatures also lower dissolved oxygen solubility. Both adversely affect microbial fuel cell performance by lowering the amount of oxygen available for as terminal electron acceptors in the catholyte. Gouveia et al. [47] observed 0.8% (w/w) (g pigment/100 g dry algae biomass) as compared to 0.6% (g pigment/100 g dry algae biomass) at higher light intensity (96 µE/m2s). Pigment content fractionation by chromatographic techniques can confirm the presence of lutein, canthaxanthin, and β-carotene. Identified chlorophyll types included chlorophyll a, b and pheophytin and pheophorbide as degradation products. Higher light intensities induced the carotenogenesis process characterized by production of β-carotene and secondary carotenoids [47,65]. Micro-algal biomass production can be accelerated under light and nutrient (nitrogen) stress [65]. The identified carotenoids (βcarotene and secondary carotenoids and lutein) have added value as antioxidants, pharmaceuticals and nutraceuticals [66]. Stimulating micro-algal growth under stress conditions can give rise to valuable compounds without compromising power output [47]. Use of blue green algae in MFCs not only produces pigments but also releases potent toxins. Micocystins are the toxins produced by blue green algae in lake waters when the algal cells rupture and die [67,68]. Micocystin cannot be treated with conventional treatment technologies such as coagulation, flocculation, sedimentation, and filtration [69,70]. Presence of blue green algae in bacterio-algal MFCs cannot effectively harvest bioelectricity but can successfully treats toxic micocystins Micocystin-RR and –LR types (90.7% and 91%) [31]. Single chamber MFC anode provides a more favourable pathway of Micocystin decomposition under anoxic condition [71]. Synthetic plastic production from algal polysaccharides is another useful product of algal biomass. Cyanobacteria is an excellent feed stock for bio-plastic production due to its high yield and ability to grow in variety of environments [72,73]. Tuccar and Aydin, [74] evaluated micro algal biodiesel in diesel engines and compared with diesel values. The results showed improved emission values however reduction in torque and brake power was observed. Mehrabadi, et al. [56] compared biodiesel quality produced from algal fatty acid methyl ester with pure diesel and concluded that biodiesel from algal fatty acid is of low quality and cannot be used directly as transportation fuel.

4.2. Cyclic voltammetry Cyclic voltammetry (CV) is used to evaluate the surface-controlled electrochemical processes that represent the redox behavior of electrochemically active microorganisms. CV applies varying potential differences across two electrodes, a working electrode and a Ag/AgCl reference electrode, allowing quantification of the electrical current generated as a result of redox reactions within the tested system which can be analysed by plotting a voltammogram [61]. In studying the behavior of bacterial-algal MFCs, Yu et al. [31] observed an oxidation peak at +0.14V and a reduction peak at -0.30V (vs. an Ag/AgCl reference electrode) and discovered that blue green algae could catalyze electron reduction at the MFC's cathode. The study also revealed proportionality in the anodic and cathodic peak currents at varying scan rates which suggested that the redox reaction was repeatable over time. Chandra et al. [59] observed marked improvement in electrochemical behavior after every feeding event in their bacterial-algal MFCs which may have been due to incremental growth in total biomass and adaptation of both anodic bacteria and cathodic algae to the system's micro-environment. Increases in oxidation peak values after fresh substrate loading was also reported by Mohan et al. [48]. Mixing produced by mechanical agitation of the catholyte solution also enhanced cathodic peak potential [29] causing voltage and current to increase by 26 mV and 4.6 mA respectively. 4.3. Electrical impedance spectroscopy Electrical impedance spectroscopy is a technique to determine the impedence response of an electrochemical system by applying an alternating circuit (AC) potential and recording the output current signal which is graphed on a Nyquist diagram, a polar plot representing a system's frequency response. Impedence is a complex combination of resistance, capacitance, and inductance effects. To determine ohmic and polarization resistance values for the studied system, a suite of standard electrical circuits are evaluated for goodness of fit to experimentally obtained impedance data. The selected equivalent circuit model consists of an ohmic resistance component (representing the MFC membrane, biofilm, and solution resistances) and polarization resistance (representing charge transfer between anode and cathode). High polarization resistance is indicated on an Nyquist diagram by an unclosed semicircle plot when analysing a complete cell (anode and cathode) and a closed semicircle plot when analysing the anodic side of the cell only. The first intersection of Nyquist plot with the x-axis represents the system's ohmic resistance, and the projected point of the intersection between the curve and the x-axis represents total impedance due to the membrane, solution, and charge transfer effects [62]. Campo [11] observed polarization resistances of 145000 Ω for a complete cell and 1069 Ω for the anode compartment only on the tenth day of operation. The results clearly indicate very high polarization resistance of the cathodic compartment as compared to the anodic polarization resistance. High polarization resistance may be due to absence of catalyst. In bacterio-algal MFCs, algae produce oxygen which accepts electrons, but the algae do not act as bioelectrical catalysts. Manohar et al. [63] also observed high cathodic polarization resistance using algae in the

5.2. Power production Pre-acclimated microorganisms in lab scale bioreactors or microbes freshly obtained from natural sources can be employed in bacterioalgal MFCs. The power output of MFCs strongly depends on low resistance in the external circuit, high permeability ion exchange membranes [41], reducing conditions, and high oxygen concentrations in the cathode chamber [2,15]. Table 1 summarizes power production potentials reported for different bacterio-algal MFCs which ranged 81

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

from 0.0033 mW/m3 to 5.2 W/m3 in maximum power output although reported units varied. Recent studies showed relatively lower power generation in bacterio-algal MFCs but these studies were performed to optimize other parameters such as effect of light intensity, seasonal effect, pigment production potential, and effect of separating the photobioreactor from the MFCs. Light intensity and duration [10], temperature [48], CO2 supply [11] are some of the parameters which strongly affect power generation and MFC efficiency. Algal biomass has been used in cathodic chamber (as phototroph and electron acceptor) and in anodic chamber (as an electron donor/substrate). Chandra et al. [59] observed 165 ± 10 mV (cycle 1) to 535 ± 10 mV (cycle 6) open circuit voltage (OCV) in a single chamber bacterio-algal MFC. Improvement in overall output was correlated with total biomass growth observed 0.55 g/L (cycle 1) to 3.24 g/L (cycle6). Power production also varied with light and dark phases of algal growth. A 350 mV drop in OCV was observed in the dark phase of algal growth [16]. Wu et al. [37] observed 99 mW/m2 power density at a current density of 380 mA/m2 employing Chlorella vulgaris in the cathodic chamber. However different algal strains behave differently [75]. Algae assisted cathodes can generate up to 1.3 times higher maximum power than non-algae assisted cathodes [76]. Variations in algal concentration did not affect OCVs 805 ± 12 mV and open circuit potentials (OCPs), anode (−537 ± 4 vs saturated calomel electrode (SCE)) and cathode (260 ± 7 vs SCE). Maximum power production from bacterio-algal MFCs varies with algal species, growth conditions and substrates, however research has proved that this type of MFC is capable of successful power production.

traditional crops including corn, canola and switchgrass and significant environmental benefits of using wastewater algae cultivation were found. Environmental and economic performance of micro-algal biofuels can not compared with traditional fossil fuels without the replacement of energy-intensive and expensive fertilizers [81,82]. 6. Limitations and summary Bacterio-algal MFC has proven to be successful at simultaneous electricity generation and wastewater treatment. Despite the potential benefits, bacterio-algal MFCs have some limitations and barriers to successful commercialization. These MFCs are affected by seasonal changes; for example Mohan et al. [48] reported observing low activity during the summer season as compared to winter. The optimal design for a bacterio-algal MFC has not yet been achieved. More detailed studies of symbiosis between the different species of microorganisms in bacterio-algal cultures are needed. This paper summarizes the most recent published research in the field of bacterio-algal MFCs, presenting power generation data along with reported sources of substrates, catholytes, and anolytes. Future developments of bacterio-algal MFCs in closed systems can provide 24 hour energy production without current limitations of catholyte replacement in non-algal MFC systems. Bacterio-algal MFCs have additional benefit of producing algal biomass which can be transformed into biofuels and other bio-products via anaerobic digestion, fermentation, or trans-esterification [89]. However to produce biomaterials and biodiesel from algal biomass needs pre-treatments and complex extraction methods which increases their price and hinders scaling up of the systems [90]. Use of algae in the anode chamber or as substrate, lowers level of out put while in the case of microalgae-assisted cathodes, the results are promising [91]. To maximize microalgae power generation much research needs to be done. Following recommendations are summarized based on the review.

5.3. Wastewater treatment Present wastewater treatment technologies are heavy users of energy, but MFCs can serve as an energy-generating wastewater pretreatment systems [14]. Wastewater can provide ample supply of nutrients, support large capacity of biofuel production and can be integrated with existing wastewater treatment infrastructure. Reduction in Chemical oxygen demand (COD) is one of the ways to measure wastewater treatment efficiency. The anaerobic consortia in an MFC's anodic chamber can easily biodegrade organic substrates and thus reduce COD. In several MFC studies, up to 90% percent COD removal was observed [8,33,48]. Table 2 summarizes reported COD removal efficiencies of bacterio-algal MFCs in the literature. Juan et al. [10] observed 80% COD removal while employing microorganisms originally collected from an oxidation ditch and supplying them with 982 mg/l and 1266 mg/L of synthetic wastewater. Gadhamshetty et al. [33] and Campo et al. [8] also observed more than 80% COD removal using wastewater microbial consortia in MFC. Mohan et al. [48] observed 74% COD removal in the anodic chamber and 58% COD removal in the cathodic chamber. Relatively few studies have studied COD removal in bacterio-algal MFCs, but it is a promising aspect of the technology that can enhance the significance and practical utilization of bacterio-algal MFC technology on a commercial scale. However, the COD removal process can be hindered by several limiting factors, including electron consumption by methanogenesis, aerobic respiration by the cathodic biofilm, and oxygen crossover [77]. Traditional activated sludge systems creates additional indirect environmental burdens in the form of sludge disposal which costs 50% of WWT operational cost. Biological nutrient removal also needs addition of tertiary treatment in WWT plant while using algae Selvaratnam et al. [78] achieved reduction in nutrient levels to regulatory discharge level. Thermophilic and acidophilic algal strains can produce double the biomass per unit nutrient intake than bacterial system and generation of 20% more net energy. 1 kg of BOD removal in algal system can generate enough biomass that can anaerobically digested to generate methane equivalent to 1 kW h of electric power [79]. Wastewater-algae life cycle assessment studies of Clarens et al. [80] compared environmental impacts of bioenergy from algae and other

1. Selection of right type of algal strain or bioengineered strain to maximize lipid production in bacterio-algal MFCs is required 2. Optimization of technological development in MFC power generation for the right kind of configuration needs more research 3. Type of biofuel and bio-oil extraction process needs to optimized for economical bio-oil production 4. Life cycle analysis of optimized MFC is required to suggest this technology on commercial scale 5. Economic life cycle assessment and optimization of MFC construction materials to propose bacterio-algal MFCs an economical technology is required 6. Integrated systems should be promoted to propose solutions of different problems such as wastewater treatment, nutrient removal, biomass pre-treatment etc. Acknowledgements Beenish Saba gratefully acknowledges a Predoctoral Fellowship from the Fulbright Program. Grant ID 17130788. References [1] Lovely DR. The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 2008;19:564–71. [2] Rismani-Yazdi H, Sarah CM, Christy AD, Tuovinen OH. Cathodic limitations in microbial fuel cells: an overview. J Power Sources 2008;180(2):683–94. [3] Logan BE. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 2009;7(5):375–81. [4] Choi C, Hu N, Cui Y, Lim B. Korean society of water and wastewater and Korean society on water quality conference. September, 2011. p. 449–450 [5] Velasquez-Orta SB, Curtis TP, Logan BE. Energy from algae using microbial fuel cells. Biotechnol Bioeng 2009:1068–76. [6] Jeon HJ, Seo KW, Lee SH, Yang YH, Kumaran RS, Kim S, Hong SW, Choi YS, Kim

82

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

[7] [8]

[9]

[10]

[11]

[12]

[13]

[14]

[15]

[16]

[17] [18]

[19]

[20] [21]

[22]

[23] [24] [25]

[26]

[27]

[28]

[29]

[30] [31]

[32]

[33]

[34] [35]

[36]

2013;15:2178–85. [37] Wu YC, Wanga Z, Zheng Y, Xiao Y, Yang Z, Zhao F. Light intensity affects the performance of photo microbial fuel cells with Desmodesmus sp. A8 as cathodic microorganism. Appl Energy 2014;116:86–90. [38] Rismani-Yazdi H, Christy AD, Dehority BA, Morrison M, Yu Z, Tuovinen OH. Electricity generation from cellulose by rumen microorganisms in microbial fuel cells. Biotechnol Bioeng 2007;97:1398–407. [39] Ganesh K, Jambeck JR. Treatment of landfill leachate using microbial fuel cells: alternative anodes and semi-continuous operation. Bioresour Technol 2013;139:383–7. [40] Walter XA, Greenman J, Ieropoulos IA. Oxygenic phototrophic biofilms for improved cathode performance in microbial fuel cells. Algal Res 2013;2:183–7. [41] Leong JX, Daud WRW, Ghasemi M, Liewa KB, Ismail M. Ion exchange membranes as separators in microbial fuel cells for bioenergy conversion: a comprehensive review. Renew Sustain Energy Rev 2013;28:575–87. [42] Ward AJ, Lewis DM, Green FB. Anaerobic digestion of algae biomass: a review. Algal Res 2014;5:204–14. [43] Ren YP, Pan DY, Li XF, Fu F, Zhao YN, Wan XH. Effect of polyaniline-graphene nanosheets modified cathode on the performance of sediment microbial fuel cell. J Chem Technol Biotechnol 2013;88:1946–50. [44] Lay CH, Marika E, Jaakko K, Puhakka A. Power generation in fed-batch and continuous up-flow microbial fuel cell from synthetic wastewater. Energy 2015;91:235–41. [45] He Z, Shao HB, Angenent LT. Increased power production from a sediment microbial fuel cell with a rotating cathode. Biosens Bioelectron 2007;22:3252–5. [46] Behera M, Jana PS, Ghangrekar MM. Performance evaluation of low cost microbial fuel cell fabricated using earthen pot with biotic and abiotic cathode. Bioresour Technol 2010;101:1183–9. [47] Gouveia L, Neves C, Sebastião D, Nobre BP, Matos CT. Effect of light on the production of bioelectricity and added-value microalgae biomass in a photosynthetic alga microbial fuel cell. Bioresour Technol 2014;154:171–7. [48] Mohan SV, Srikanth S, Chiranjeevi P, Arora S, Chandra R. Algal biocathode for in situ terminal electron acceptor (TEA) production: synergetic association of bacteria–microalgae metabolism for the functioning of biofuel cell. Bioresour Technol 2014;166:566–74. [49] Harper CA, Sampson RM. Electronic materials and process handbook. Newyork: McGraw Hill; 1994. [50] Myerse J. On the algae: thoughts about physiology and measurements of efficiency primary productivity in the sea. Environemntal Sceince Resaerch, 19. US: Springer; 1980. p. 1–16. [51] Cao XX, Huang X, Liang P, Xiao K, Zhou YJ, Zhang XY, Logan BE. A new method for water desalination using microbial desalination cells. Environ Sci Technol 2009;43:7148–52. [52] Zhang X, Xia X, Ivanov I, Huang X, Logan BE. Enhanced activated carbon cathode performance for microbial fuel cell by blending carbon black. Environ Sci Technol 2014;48:2075–81. [53] Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS. Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 2009;100:833–8. [54] Liu J, Huang J, Sun Z, Zhong Y, Jiang Y, Chen F. Differential lipid and fatty acid profiles of photoautotrophic and heterotrophic Chlorella zofingiensis: assessment of algal oils for biodiesel production. Bioresour Technol 2011;102:106–10. [55] Ho SH, Chen WM, Chang JS. Scenedesmus obliquus CNW-N as apotential candidate for CO2 mitigation and biodiesel production. Bioresour Technol 2010;101:8725–30. [56] Mehrabadi A, Craggs R, Farid MM. Biodiesel production potential of wastewater treatment high rate algal pond biomass. Bioresour Technol 2016;221:222–33. [57] Biffinger JC, Byrd JN, Dudley BL, Ringeisen BR. Oxygen exposure promotes fuel diversity for Shewanella oneidensis microbial fuel cells. Biosens Bioelectron 2008;23:820–6. [58] Rodrigo MA, Cañizares P, Lobato J. Effect of the electron-acceptors on the performance of a MFC. Bioresour Technol 2010;101:7014–8. [59] Chandra R, Subhash GV, Mohan SV. Mixotrophic operation of photo-bioelectrocatalytic fuel cell under anoxygenic microenvironment enhances the light dependent bioelectrogenic activity. Bioresour Technol 2012;109:46–56. [60] Jiang J, Zhao Q, Zhang J, Zhang G, Lee D. Electricity generation from biotreatment of sewage sludge with microbial fuel cell. Bioresour Technol 2009;100:5808–12. [61] Evans DH, O’Connell KM, Petersen RA, Kelly MJ. Cyclic voltammetry. Chem Educ 1983;60(4):290–3. [62] Borole AP, Aaron D, Hamilton CY, Tsouris C. Understanding Long-Term Changes in Microbial Fuel Cell Performance Using Electrochemical Impedance Spectroscopy. Environ Sci Technol 2010;44:2740–5. [63] Manohar AK, Bretschger O, Nealson KH, Mansfeld F. The use of electrochemical impedance spectroscopy (EIS) in the evaluation of the electrochemical properties of a microbial fuel cell. Bioelectrochemistry 2008;72:149–54. [64] Berman T, Holm-Hansen O. Release of photoassimilated carbon as dissolved organic matter by marine phytoplankton. Mar Biol 1974;28:305–10. [65] Campenni' L, Nobre BP, Santos CA, Oliveira AC, Aires-Barros MR, Palavra AMF. Carotenoid and lipid production by the autotrophic microalga Chlorella protothecoides under nutritional, salinity, and luminosity stress conditions. Appl Microbiol Biotechnol 2013;97:1383–93. [66] Maiani G, Castón MJP, Catasta G, Toti E, Cambrodón IG, Bysted A, GranadoLorencio F, Olmedilla-Alonso B, Knuthsen P, Valoti M, Böhm V, Mayer-Miebach E, Behsnilian D, Schlemmer U. Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol Nutr

HJ. Roduction of algal biomass (Chlorella vulgaris) using sediment microbial fuel cells. Bioresour Technol 2012;109:308–11. Melis A, Melnicki MR. Integrated biological hydrogen production. Int J Hydrog Energy 2006;31:1563–73. Cui Y, Rashid N, Hu N, Rehman MSU, Han JI. Electricity generation and microalgae cultivation in microbial fuel cell using microalgae-enriched anode and bio-cathode. Energy Convers Manag 2014;79:674–80. Rashid N, Cui Y, Rehman MS, Han JI. Enhanced electricity generation by using algae biomass and activated sludge in microbial fuel cell. Sci Total Environ 2013:456–7. Juang DF, Lee CH, Hsueh SC. Comparison of electrogenic capabilities of microbial fuel cell with different light power on algae grown cathode. Bioresour Technol 2012;123:23–9. Campo GAD, Cañizares P, Rodrigo MA, Fernández FJ, Lobato J. Microbial fuel cell with an algae-assisted cathode: a preliminary assessment. J Power Sources 2013;242:638–45. Tugtas AE, Cavdar P, Calli B. Continuous flow membraneless air cathode microbial fuel cell with spunbonded olefin diffusion layer. Bioresour Technol 2011;102:10425–30. Li XM, Cheng KY, Wong JWC. Bioelectricity production from food waste leachate using microbial fuel cells: effect of NaCl and pH. Bioresour Technol 2013;149:452–8. Wang X, Feng Y, Liu J, Lee J, Li C, Li N, Ren N. Sequestration of CO2 discharged from anode by algal cathode in microbial carbon capture cells (MCCs). Biosens Bioelectron 2010;25:2639–43. Lobato J, Campo GAD, Fernández FJ, Cañizares P, Rodrigo MA. Lagooning microbial fuel cells: a first approach by coupling electricity-producing microorganisms and algae. Appl Energy 2013;110:220–6. Gajda I, Greenman J, Melhuish C, Ieropoulos I. Self-sustainable electricity production from algae grown in a microbial fuel cell system. Biomass Bioenergy 2015;82:87–93. Nishio K, Hashimoto K, Watanabe K. Light/electricity conversion by defined cocultures of Chlamydomonas and Geobacter. J Biosci Bioeng 2013;115:412–7. Richardson JM, Johnson MD, Outlaw JL. Economic comparison of open pond raceways to photo bio-reactors for profitable production of algae for transportation fuels in the Southwest. Algal Res 2012;1:93–100. Murphy F, Devlin G, Deverell R, McDonnell K. Biofuel Production in Ireland—an approach to 2020 targets with a focus on algal biomass. Energies 2013;6:6391–412. High CF. Cell density culture of microalgae in heterotrophic growth. Trends Biotechnol 1996;14:421–6. Cuaresma M, Janssen M, Vilchez C, Wijffels RH. Productivity of Chlorella sorokiniana in a short light-path (SLP) panel photo-bioreactor under high irradiance. Biotechnol Bioeng 2009;104:352–9. El-Mekawy A, Hegab HM, Vanbroekhoven K, Pant D. Techno-productive potential of photosynthetic microbial fuel cells through different configurations. Renew Sustain Energy Rev 2014;39:617–27. Campos-Martin JM, Blanco-Brieva G, Fierro JLG. Hydrogen peroxide synthesis: an outlook beyond the anthraquinone process. Angew Chem Int Ed 2006;45:6962–84. Powell EE, Mapiour ML, Evitts RW, Hill GA. Growth kinetics of Chlorella vulgaris and its use as a cathodic half-cell. Bioresour Technol 2009;100:269–74. Lin CC, Wei CH, Chen CI, Shieh CJ, Liu YC. Characteristics of the photosynthesis microbial fuel cell with a Spirulina platensis biofilm. Bioresour Technol 2013;135:640–3. Fu CC, Hung TC, Wu WT, Wen TC, Su CH. Current and voltage responses in instant photosynthetic microbial cells with Spirulina platensis. Biochem Eng J 2010;52:175–80. Fu CC, Su CH, Hung TC, Hsieh CH, Suryani D, Wu WT. Effects of biomass weight and light intensity on the performance of photosynthetic microbial fuel cells with Spirulina platensis. Bioresour Technol 2009;100:4183–6. Wang ZJ, Deng H, Chen LH, Xiao Y, Zhao F. In situ measurements of dissolved oxygen, pH and redox potential of biocathode microenvironments using microelectrodes. Bioresour Technol 2013;132:387–90. Kakarla R, Min B. Photoautotrophic microalgae Scenedesmus obliquus attached on a cathode as oxygen producers for microbial fuel cell (MFC) operation. Int J Hydrog Energy 2014;39:10275–83. Demribas MF. Biofuels from algae for sustainable development. Appl Energy 2011;88(10):3473–80. Yuan Y, Chena Q, Zhoua S, Zhuanga L, Hu P. Bioelectricity generation and microcystins removal in a blue-green algae powered microbial fuel cell. J Hazard Mater 2011;187:591–5. Chandra R, Subhash GV, Mohan SV. Mixotrophic operation of photo-bioelectrocatalytic fuel cell under anoxygenic microenvironment enhances the light dependent bioelectrogenic activity. Bioresour Technol 2012;109:46–56. Gadhamshetty V, Belanger D, Gardiner CJ, Cummings A, Hynes A. Evaluation of Laminaria-based microbial fuel cells (LbMs) for electricity production. Bioresour Technol 2013;127:378–85. Gajda I, Greenman J, Melhuish C, Ieropoulos I. Photosynthetic cathodes for microbial fuel cells. Int J Hydrog Energy 2013;38:11559–64. Saba B, Christy AD. Comparison of biological catholyte to chemical catholyte in microbial desalination cells. In : Proceedings of annual international mieeting of American Society of Agricultural and Biological Engineers (ASABE). July, 26–29, New Orleans Lousiana, USA (doi: http://dx.doi.org/10.13031/aim.20152190931) Paper number 152190931; 2015. Kokabian B, Gude VG. Photosynthetic microbial desalination cells (PMDCs) for clean energy: water and biomass production. Environ Sci Process Impacts

83

Renewable and Sustainable Energy Reviews 73 (2017) 75–84

B. Saba et al.

Micro-algal biotechnology.. Cambridge University Press; 1988. p. 305–28. [80] Clarens AF, Resurreccion EP, White MA, Colosi LM. Environmental life cycle comparison of algae to other bioenergy feedstocks. Environ Sci Technol 2010;44(5):1813–9. [81] Davis R, Aden A, Pienkos PT. Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energy 2011;88(10):3524–31. [82] Gallagher BJ. The economics of producing biodiesel from algae. Renew Energy 2011;36:158–62. [83] Dewan A, Beyenal H, Lewandowski Z. Scaling up microbial fuel cells. Environ Sci Technol 2008;42:7643–8. [84] Logan B, Watson SV, Estadt G. Graphite fiber brush anodes for increased power production in air-cathode microbial fuel cells. Environ Sci Technol 2007;41(9):3341–6. [85] Tsai HY, Wu CC, Lee CY, Shih EP. Microbial fuel cell performance of multiwall carbon nanotubes on carbon cloth as electrodes. J Power Sources 2009;194(1):199–205. [86] Kim HJ, Parka HS, Hyunb MS, Changa IS, Kima M, Kim BH. A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enzyme Micro Technol 2002;30(2):145–52. [87] Magrez A, Kasas S, Salicio V, Pasquier N, Seo JW, Celio M, Catsicas S, Schwaller B, Forró L. Cellular Toxicity of Carbon-Based Nanomaterials. Nano Lett 2006;6(6):1121–5. [88] Zhang X, Amendola P, Hewson JC, Sommerfeld M, Hu Q. Influence of growth phase on harvesting of Chlorella zofingiensis by dissolved air flotation. Bioresour Technol 2012;116:477–84. [89] Baicha Z, Salar-Garcia MJ, Ortiz-Martinez VM, Hernandez-Fernandez FJ, De los Rios AP, Labjar N, Lotfi E, Elmahi M. A critical review on microalgae as an alternative source for bioenergy production: a promising low cost substrate for microbial fuel cells. Fuel Process Technol 2016;154:104–16. [90] Hoh D, Watson S, Kan E. Algal biofilm reactors for integrated wastewater treatment and biofuel production: a review. Chem Eng J 2016;287:466–73. [91] Saba B, Christy AD, Yu Z, Co AC, Tuovinen OH, Islam R. Characterization and performance of anodic mixed culture biofilms in submersed microbial fuel cells. Bioelectrochemistry 2017:113. http://dx.doi.org/10.1016/j.bioelechem.2016.10.003.

Food Res 2009;53(2):194–218. [67] Pouria S, Andrade AD, Cavalcanti RL, Barreto VT, Ward CJ, Preiser W, Poon GK, Neild GH, Codd GA. Fatal microcystin intoxication in haemodialysis unit in Caruaru, Brazil. Lancet 1998;352:21–6. [68] Romanowska-Duda Z, Mankiewicz J, Tarczynska M, Walter Z, Zalewski M. The effect of toxic cyanobacteria (blue-green algae) on water plants and animal cells. Pol J Environ Stud 2002;11:561–6. [69] Himberg K, Keijola AM, Hiisvirta L, Pyysalo H, Sivonen K. The effect of water treatment processes on the removal of hepatotoxins from Microcystis and Oscillatoria cyanobacteria: a laboratory study. Water Res 1989;23(8):979–84. [70] Chow CWK, Drikas M, House J, Burch MD, Velzeboer RMA. The impact of conventional water treatment processes on cells of the cyanobacterium Microcystis aeruginosa. Water Res 1999;33:3253–62. [71] Holst T, Jørgensen NOG, Jørgensen C, Johansen A. Degradation of microcystin in sediments at oxic and anoxic denitrifying conditions. Water Res 2003;37:4748–60. [72] Seiichi T, Doi Y. Evolution of polyhydroxyalkanoate (PHA) production system by enzyme evolution: successful case studies of directed evolution. Macromol Biosci 2004;3:145–56. [73] Sudesh K, Abe H, Doi Y. Synthesis, structure and properties of polyhydroxyalkanoates: biological polyesters. Prog Polym Sci 2000;25:1503–55. [74] Tuccar G, Aydin K. Evaluation of methyl ester of microalgae oil as fuel in a diesel engine. Renew Sustain Energy Rev 2013;112:203–7. [75] McCormick AJ, Bombelli P, Scott AM, Philips AJ, Smith AG, Fisher AC. Photosynthetic biofilms in pure culture harness solar energy in a mediatorless biophotovoltaic cell (BPV) system. Energy Environ Sci 2011;4:4699–709. [76] Wang H, Laughinghouse HD, Anderson MA, Chen F, Willliams E, Place AR, Zmora O, Zohar Y, Zheng T, Hill RT. Novel bacterial isolate from Permian groundwater, capable of aggregating potential biofuel-producing microalga Nannochloropsis oceanica IMET1. Appl Environ Microbiol 2012;78:1445–53. [77] Liu H, Cheng S, Logan BE. Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environ Sci Technol 2005;39:658–62. [78] Selvaratnam T, Pegallapati A, Montelya F, Rodriguez G, Nirmalakhandan N, Lammers PJ, Voorhies WV. Feasibility of algal systems for sustainable wastewater treatment. Renew Energy 2015;82:71–6. [79] Oswald WJ. Microalgae and waste-water treatment. In: Borowitzka MBL, editor.

84