8TH ASIAN PACIFIC PHYCOLOGICAL FORUM

Algal biophotovoltaic (BPV) device for generation of bioelectricity usingSynechococcus elongatus (Cyanophyta)

Fong-Lee Ng1& Siew-Moi Phang1,2

& Vengadesh Periasamy3 & John Beardall4 & Kamran Yunus5 & Adrian C. Fisher5

Received: 25 January 2018 /Revised and accepted: 14 May 2018# Springer Science+Business Media B.V., part of Springer Nature 2018

AbstractThe exploitation of renewable energy sources for delivering carbon neutral or carbon negative solutions has become challengingin the current era because conventional fuel sources are of finite origins. Algae are being used in the development ofbiophotovoltaic (BPV) platforms which are used to harvest solar energy for bioelectricity generation. Fast-growing algae havea high potential for converting CO2 from the atmosphere into biomass and valuable products. In photosynthesis light-drivensplitting of water occurs, releasing a pair of electrons and generating O2. The electrons can be harvested and converted tobioelectricity. In this study, algal biofilms of a tropical cyanobacterial strain Synechococcus elongatus (UMACC 105) wereformed on two types of electrodes, indium tin oxide (ITO) and reduced graphene oxide (rGO), and investigated for use in thealgal biophotovoltaic (BPV) device. The highest maximum power density was registered in the rGO-based BPV device (0.538 ±0.014 mWm−2). This illustrates the potential of this local algal strain for use in BPV devices to generate bioelectricity in both thelight and dark conditions.

Keywords Algal biophotovoltaic (BPV) device . Bioelectricity . Cyanophyta

Introduction

Sunlight is the most abundant and sustainable source of ener-gy available to humanity. Annual solar energy production isapproximately 120,000 TWand estimated to be about 20,000times more than the present annual energy consumption of theworld (Blankenship et al. 2011). There is a huge drive to

develop low carbon technologies and how to capture and storeradiant energy for societal use is one of the greatest challengesof our age. The total amount of biomass produced by photo-synthesis is equivalent to 4 × 1021 J of energy, approximately10 times the total annual global energy consumption (Helmut2005). Algae are known to be one of the most photosynthet-ically efficient organisms, harnessing solar energy into theproduction of a diverse range of products such asbiopharmaceuticals and bioenergy (Lim et al. 2010).

Cyanobacteria (Cyanophyta) or blue green algae are a dis-tinct group of photosynthetic organisms. They are the onlyprokaryotes with oxygenic photosynthesis. Cyanobacteriaare prokaryotes and as such the energy-transducing mem-branes are not located in mitochondria or chloroplasts as inhigher plants. They are contained in a densely packed mem-brane system (thylakoids) in the cytoplasm (Binder 1982).Cyanobacteria generally harness 0.2 to 0.3% of the solar en-ergy. The amount of energy that passes through thecyanobacteria exceeds by more than 25 times the energy de-mand of human populations and an estimated 1000 times theenergy produced by all the nuclear plants on Earth. On aglobal scale, Cyanobacteria fix an estimated 25 Gigatonnesof carbon from CO2 per year into energy-dense biomass(Pisciotta et al. 2010).

* Fong-Lee Ngfonglee_ng@yahoo.com

* Siew-Moi Phangphang@um.edu.my

1 Institute of Ocean and Earth Sciences (IOES), University of Malaya,50603 Kuala Lumpur, Malaysia

2 Institute of Biological Sciences, Faculty of Science, University ofMalaya, 50603 Kuala Lumpur, Malaysia

3 Low Dimensional Materials Research Centre (LDMRC),Department of Physics, University of Malaya, 50603 KualaLumpur, Malaysia

4 School of Biological Sciences, Monash University,Clayton, Victoria 3800, Australia

5 Department of Chemical Engineering and Biotechnology, Universityof Cambridge, Philipa Fawcett Drive, Cambridge CB3 0AS, UK

Journal of Applied Phycologyhttps://doi.org/10.1007/s10811-018-1515-1

Investigation of photosynthetic bacteria and their applica-tion in power generation has led to the development of a rangeof photo-microbial fuel cells. High-energy electrons producedby the light excitation in the photosystems are transferred to anelectron mediator, which in turn transfers them to an electrodeand thereby producing electricity (Quintana et al. 2011).Recent studies have reported the use of cyanobacteria for hy-drogen generation (Prince and Kheshgi 2005) and electricitygeneration using 2-hydroxy-1,4-naphthoquinone as an elec-tron shuttle between the algae cells and a carbon-cloth anode(Yagishita et al. 1997). Other studies have explored the use ofbioreactors with an air cathode and a graphite-felt anode coat-ed by a biofilm of bacteria and algae, which generates elec-tricity when irradiated (Nishio et al. 2010). Electrical energycan also be extracted directly from photosynthetic algae usingbiophotovoltaic (BPV) devices (Bombelli et al. 2011). Thesynergistic interaction between anoxygenic and oxygenicphotosynthesis and the electrogenic activity of this photo-bioelectrocatalytic fuel cell has also been reported. A systemcombining microbial fuel cell and a photobioreactor, whichgenerated a maximum power density of 20.3Wm−3, has beendeveloped for bioelectricity generation and for continuous do-mestic wastewater treatment (Jiang et al. 2012).

The use of BPV cells based on algal biofilms cultivated atthe electrode surfaces is a key element in improving BPVdevices and exploring them as a potential source of renewableand sustainable electrical energy (Kim et al. 2006). Previously,BPV studies have utilized various exogenous soluble media-tor compounds to facilitate electron transfer. McCormick et al.(2011) avoided the use of exogenous mediators by developingand utilizing biofilms. We previously reported using biofilmsof two species of the Chlorophyta genus Chlorella and twospecies of cyanobacteria Arthrospira (Spirulina) andSynechococcus elongatus, on indium-tin-oxide (ITO) anodesand obtained increased power output ranging from 1.12 ×10−4 to 3.13 × 10−4 W m−2 (Ng et al. 2014a). Replacing ITOelectrodes with reduced graphene oxide (rGO) anode andusing a green alga, Chlorella sp., power output was furtherincreased by 119% (0.148 mW m−2) compared to the formerITO anode (Ng et al. 2014b). ITO and rGOwere utilized as thepotential anode materials in this project for the fabrication ofsuitable BPV devices. ITO was an early favorite with goodtransparency and conductivity (Hwang et al. 2006), while rGOis highly conductive, flexible, and has controllable permittiv-ity and hydrophilicity (Kostarelos and Novoselov 2014).Changes in the physical environment were monitored to ob-serve the effects on power output of the BPV devices.Maximum power density was observed when Chlorella sp.was immobilized in alginate gel within a fuel cell: an increaseof 18% in power output compared to conventional suspensionculture BPV devices with 0.289 mW m−2 (Ng et al. 2017). Inthe present work, we investigate the potential of a cyanobac-terium, S. elongatus, as a candidate in ITO- and rGO-based

BPV devices, compare this with the power output ofchlorophytes, Chlorella sp., reported previously.

Materials and methods

Algal culture

A local tropical cyanobacterial strain from the University ofMalaya Algae Culture Collection (UMACC) Synechococcuselongatus (UMACC 105) was selected for this study. An in-oculum size of 20%, standardized at an OD of 0.2 at 620 nm(OD620nm) from exponential phase cultures, was used. Thecultures were grown in Kosaric Medium (Phang and Chu1999). The cultures were grown in 1-L conical flasks in anincubator shaker (120 rpm) at 25 °C, with an irradiance of40 μmol photons m−2 s−1 on a 12:12 light-dark cycle. Thecyanophyte was grown in triplicates with a total culture vol-ume of 500 mL.

Algal biofilm formation of S. elongatus on indium tinoxide anodes and reduced graphene oxide anodes

Synechococcus elongatus (UMACC 105) was used for thebiofilm studies, based on its ability to form biofilm (Ng etal. 2014a). One hundred milliliter of exponential phase cul-tures of OD620nm = 0.5 were used. Each culture was placedinto a 200-mL autoclaved glass staining jar. Indium tin oxide(ITO)-coated glass slides (KINTEC, HongKong) and reducedgraphene oxide (rGO) anodes (Ng et al. 2014b) measuring35 × 35 mm were placed in a staining jar with the microalgaeculture and transferred into an incubator at 24 °C illuminatedby cool white fluorescent lamps (40 μmol photons m−2 s−1) ona 12:12 h light-dark cycle to allow for the algae biofilms toform on the slides. The experiments were conducted in tripli-cates for 15 days.

BPV device set-up and electrical measurement usingindium tin oxide and reduced graphene oxide anodes

The rGO anode was fabricated using the Langmuir-Blodgettmethod as shown in our previous study (Ng et al. 2014b). Theclosed, single-chamber BPV consisted of a 50 × 50-mmplatinum-coated glass cathode placed in parallel with 35 ×35 mm ITO- or rGO-coated glass. Biofilms were grown onthe surface (10 mm apart) in a clear Perspex chamber sealedwith PDMS and the cavity filled with medium. The body ofthe open-air and single-chamber BPVwas constructed of clearPerspex. Biofilms of S. elongatus grown on the ITO- andrGO-coated glasses were then placed in the BPV device.Crocodile clips and copper wire were used and served as theconnection between anode and cathode to the external circuit.Figure 1 shows the stepwise set-up of the BPV device.

J Appl Phycol

For light measurement, the BPV devices were placed underirradiances of 40 μmol photons m−2 s−1 for the duration of theexperiments. For dark measurement, BPV devices wereplaced in a dark room and the device covered with a blackcloth. The chambers were filled with fresh medium and main-tained at 25 °C. Light meter (LI-250A, Licor) was used toconfirm the device was in the dark. After dark adaptation for15 min, current outputs were measured using a multimeter(Agilent U1251B). Polarization curves were generated foreach strain by applying different resistance (10 MΩ,5.6 MΩ, 2 MΩ, 560 KΩ, 240 KΩ, 62 KΩ, 22 KΩ, 9.1 KΩ,3.3 KΩ, and 1.1 KΩ) loads to the external circuit. All exper-iments were conducted in triplicates and standard deviationswere calculated.

Chlorophyll-a concentration

On day 15 the algal biofilms on the anodes were removed bywashing using jets of distilled water from a pipette and ana-lyzed for their Chl-a content. The Chl-a concentration wasevaluated using spectrophotometric method (Strickland andParsons 1968). The algal cells removed from ITO and rGOanodes and filtered on to filter paper (Whatman GF/C,0.45 μm) and the papers were mashed using a tissue grinder(Kimble, USA) with 10 mL of analytical grade 100% acetone.

The samples were then left in a freezer (4 °C) for 24 h beforebeing centrifuged (1509×g, 10 min, 4 °C). Absorption of thesupernatant was measured at the wavelengths of 630 nm(OD630nm), 645 nm (OD645nm), and 665 nm (OD665nm).

The Chl-a concentration was calculated using the follow-ing formula:

Chl−a mg m‐3� � ¼ Ca � Vað Þ=Vc

where Ca = 11.6 × OD665nm − 1.31 × OD645nm − 10.14 ×OD630nm, Va = Volume of acetone (mL) used for extraction,

Vc ¼ Volume of culture Lð Þ;Chl‐a mg L‐1� �

¼ Chl‐a mg m‐3� �

=1000:

Chronoamperometry measurements

A PAR-VersaSTAT two-electrode electrochemical worksta-tion was used to perform chronoamperometry to study theelectrochemical stability of the anodes based on ITO andrGO. The experiment was performed at room temperature(25 °C) under light and dark conditions. To perform the char-acterization in dark, BPV devices were placed in a dark roomand the device covered with a black cloth. To confirm the

Fig. 1 Stepwise set-up of the BPV device

J Appl Phycol

device was in the dark without any light source, a light meter(LI-250A, Licor) was used to detect the light intensity of thedevice environment and the reading was found to be zero. Forlight measurements, BPV devices were illuminated using lightsource with an irradiance of 100 μmol photons m−2 s−1.(Strycharz-Glaven et al. 2013; Ibrahim et al. 2018).

Results

Ng et al. (2014b) used the green microalga (Chlorella sp.) andreplaced ITO with rGO anode into a BPV device. Under lightconditions, a higher power output was generated in the rGO-based BPV with a value of 0.273 ± 0.025 mW m−2. In thepresent study, we grew biofilms of the cyanobacterium S.elongatus with the same rGO-based anode BPV device andobtained higher power output of 0.520 ± 0.011 mW m−2. Inthe ITO-based anode BPV device, there was an increase of0.197 mWm−2 (157.6%) in light and 0.082 mWm−2 (52.8%)in dark conditions. In the rGO-based BPV, there was an in-crease of 0.247 mW m−2 (47.5%) in the light and0.327 mW m−2 (60.8%) in the dark.

Table 1 shows the details of the power output for ITO andrGO-based BPV devices in light and dark conditions for S.elongatus. Figures 2 and 3 demonstrate the polarization curvesof S. elongatus in ITO and rGO-based BPV devices, respec-tively. Higher power output was observed from the rGO-basedBPV compared to the ITO-based BPV device, similar to ourprevious study (Ng et al. 2014b). In the light condition, therewas an increase of power output from 0.322 to 0.520 mWm−2

(61.49%) for rGO compared to ITO-based electrodes. In thedark condition, the power output was increased from 0.156 to0.538 mW m−2 (244.87%) for the rGO compared to ITO-based BPV device.

In our current study, power output-based on algal biomass(using Chl-a content) was est imated as 0.139 ±0.025 mW m−2 μg−1 Chl-a generated in light condition and(0.067 ± 0.002) mWm−2 μg−1 Chl-a generated in dark condi-tion for the ITO-based BPV device. For the rGO devices,0.212 ± 0.014 mW m−2 μg−1 of Chl-a was generated in lightand 0.219 ± 0.025 mW m−2 μg−1 Chl-a in dark conditions.These values were obtained by dividing the maximum powerdensity by the total Chl-a content in the BPV device(ANOVA, Tukey’s HSD test, p < 0.05).

Discussion

BPV systems have many possible electron-transfer steps be-tween the water photolysis processes to electrons donationprocess at the anode. It encompasses a broad range of tech-nologies, employing biological materials that can harness lightenergy to split water and transfer the resulting electrons to an

anode for bioelectricity generation (Bradley et al. 2012).Green microalgae and cyanobacteria are oxygenic photosyn-thetic microorganisms which contain chlorophyll to absorbsolar energy and convert it into chemical energy. This processinvolves splitting water to oxygen and protons (H+). For thegreen microalgae complex, redox reaction occurs in the thy-lakoid of chloroplasts and for cyanobacteria this process hap-pens in the thylakoid membranes in the cytoplasm. The pho-tosynthetic electron transfer involves light and dark reactions.The light reactions are involved in obtaining electrons bysplitting water in Photosystem II (PS II). Electrons are trans-ferred through an electron transport chain from PSII via theplastoquinone (PQ) pool, cytochrome b6f complex (Cyt b6f),photosystem I (PSI) to ferredoxin (Fd), resulting in the gener-ation of adenosine triphosphate (ATP) and nicotinamide ade-nine dinucleotide phosphate (NADPH) (Khetkorn et al. 2017).

Photolysis can be considered as a complicated process inthylakoid membranes located in chloroplast system.Efficiency will be decreased due to energy lost when the elec-tron is passed between carrier molecules. Cyanobacteria havea comparatively simple internal structure compared to greenmicroalgae, the thylakoid membranes where charge separa-tion occurs are directly exposed to the cytoplasm.Cyanobacterial thylakoids contain components of respiratoryelectron transport as well as photosynthetic electron, some ofwhich are shared between the two processes, and contain mo-lecular components (a hypothetical NADPH/mediator oxido-reductase) which generate equivalents from light or fromstored metabolites and may contribute to current generation(Bradley et al. 2012).

In the ITO-based BPV, the power output is higher in thelight compared to the dark condition while rGO-based BPVshowed the opposite behavior. The rGO-based BPV in darkcondition was higher than in the light condition. There was aslight increase of 0.018 mW m−2 (3.46%) in darkness com-pared to in the light in the rGO-based BPV device. In the darkreactions of photosynthesis (Calvin Cycle), CO2 is fixed andreduced into organic compounds in the form of starch (ingreen algae) or glycogen (in cyanobacteria) by using chemicalenergy obtained from the light reactions. In the dark,cyanobacteria will satisfy their need for energy with respira-tion. As stated above, in cyanobacteria, these mitochondrial-like aerobic respiration reactions occur in the same energy-transducing membranes as the light reaction of photosynthesis(Allahverdiyeva et al. 2014). The combination of the darkreactions in cyanobacteria and the improved power output inan rGO anode (Ng et al. 2014b) contributed to thisphenomenon.

Chronoamperometry was conducted to investigate the sta-bility of rGO- and ITO-based anodes towards the photocurrentgeneration at 0.8-V applied potential as shown in Fig. 4.Evident from the figure, both ITO and rGO-based anodesshowed an insignificant current response in the dark. The

J Appl Phycol

rGO-based anode exhibited improved current response in lightas well as dark conditions as compared to ITO. The currentresponse of all samples used in this study remained at a con-stant level throughout the experiment, showing robustness andhigh stability of the samples studied.

Growth is very slow in the dark and all the respiratoryactivities, including oxidative phosphorylation, are lowercompared to the corresponding rates in the light (photosyn-thetic electron transport and photophosphorylation).Respiration allows algae to cope in the dark by using minimalenergy metabolism in order to survive (Binder 1982).Photosynthetic efficiency of algae can decrease and not oper-ate efficiently in too high light conditions, if the ratio of an-tenna to reaction centers is too high and this will result inexcess light absorption and wastage (Benemann 1997).Cyanobacteria have strict light requirements and a high lightflux will damage the cells though in contrast too low a lightflux can result in insufficient energy production and cells re-sort to heterotrophic respiration (Tamulonis et al. 2011).

Some cyanobacterial strains are capable of assimilatingsugars and growth in dark conditions as facultative hetero-trophs. Respiration and photosynthesis co-occur in a singlecompartment within the cyanobacterial cells in the thylakoidmembrane (Quintana et al. 2011). In the light, H2O and CO2

are converted into glucose. In the dark, glucose will be usedfor metabolic activities for internal biological functions in-volved in maintenance and growth (Furukawa et al. 2005).Although the constituents from both electron transfer chainssuch as the redox carriers cytochrome bf complex, plastoqui-none, cytochrome c6, and plastocyanin are shared. Althoughthey have common elements, some of them are still specifi-cally associated to one of the pathways. PSI and PSII com-plexes are photosynthesis specific, whereas NADP dehydro-genase, succinate dehydrogenase, and terminal oxidases occuronly in the respiratory chain (Quintana et al. 2011).

A number of cyanobacterial strains have been shown to becapable of heterotrophic growth dependent solely on exoge-nous reduced organic compounds, metabolized via the

Fig. 2 Polarization curves of Synechococcus elongatus in ITO-based BPV devices (n = 3)

Table 1 Power outputs for ITO- and rGO-based BPV devices in light and dark conditions for Synechococcus elongatus (UMACC 105); data as means± S.D. (n = 3). Differences between letters indicate significant difference between different strains (ANOVA, Tukey’s HSD test, p < 0.05)

Anodematerial

Condition Maximum currentdensity (mA m–2)

Maximum powerdensity (mW m–2)

Maximum currentdensity (mAm–2) μg–1 Chl-a

Maximum powerdensity (mW m–2) / μg Chl-a

ITO Light 2.929 ± 0.007b 0.322 ± 0.005b 1.266 ± 0.084b 0.139 ± 0.025b

Dark 1.785 ± 0.008c 0.156 ± 0.008c 0.772 ± 0.078c 0.067 ± 0.002c

rGO Light 3.622 ± 0.001ab 0.520 ± 0.011a 1.479 ± 0.051ab 0.212 ± 0.014a

Dark 4.171 ± 0.006a 0.538 ± 0.014a 1.701 ± 0.215a 0.219 ± 0.025a

J Appl Phycol

oxidative pentose-phosphate cycle (Pelroy and Bassham1972). Cyanobacteria are able to reduce these organic com-pounds for supporting heterotrophic growth (Smith 1982).Anderson and McIntosh (1991) reported that the unicellularc y a n o b a c t e r i um S y n e c h o c y s t i s s p . c a n g r owphotoheterotrophically at the expense of glucose as a sourceof reduced organic carbon, without the need for a functionalPSII (Anderson and McIntosh 1991). Tanaka et al. (1985)reported bioelectrochemical fuel cells operated in anaerobiccondition using the cyanobacterium Anabaena variabilis.

Their results indicated a 0.4-V power output generated in thedark with a fixed load (400 Ω) and demonstrated that theelectricity source obtained from the fuel cells is endogenousglycogen in the dark and glycogen and electrons producedfrom photosynthetic oxidation of water in the light (Tanakaet al. 1985). Chiao et al. (2006) reported that cyanobacteria ina photosynthetic electrochemical cell produced electrons byphotosynthetic reactions under light and continued to generatepower under darkness using glucose (0.04 nW cm−2), andgenerated electricity from both photosynthesis and catabolism

Fig. 3 Polarization curves of Synechococcus elongatus in rGO-based BPV devices (n = 3)

Fig. 4 Chronoamperometrymeasurements for ITO- and rGO-based anodes obtained under lightand dark conditions at 0.8-Vapplied potential

J Appl Phycol

of endogenous carbohydrates in light and from catabolismalone in dark (Chiao et al. 2006).

He et al. (2009) reported that a sediment-type self-sustained phototrophic microbial fuel cell registered an in-creased electric current in the dark and a decreased currentwith the light. The current started to increase and reach ahighest value of 0.054 ± 0.002 mA. The current increased inthe dark and decreased with the light on, possibly becauseof the negative effect of the oxygen produced via photosyn-thesis. During an extended dark period the current increasedbecause of the oxidation of organic compounds that accu-mulated during the light reactions, and then decreased be-cause of the depletion of easily metabolized organics (He etal. 2009).

Pisciotta et al. (2010) investigated the light-dependentelectrogenic activity of Synechococcus sp., based on its ca-pability to deposit electrons to the extracellular environ-ment (anode materials) in response to illumination. Theyobserved the ability of the cyanobacterium to donate elec-trons directly to the anode. This response was mediated bySynechococcu s sp . b e c au s e an anode w i t hou tcyanobacterial cells displayed no such response. From ourprevious study (Ng et al. 2014b), modification of the nano-structure on of the anode surface can improve the poweroutput of BPV devices as shown by the 118% enhancementwhen using the rGO anode. This finding is similar to theirfindings, which reported that the yield of electron harvest-ing could be improved by as much as 4.5-fold simply bychanging the nanostructure of the anode surface. Other fac-tors such as the chemical environment, the physical prop-erties of the electron acceptors, solar radiation intensity, andthe dissolved oxygen concentration might also affect theelectron discharge (Pisciotta et al. 2010).

Conclusions

The power output of Synechococcus elongatus was highercompared to Chlorella sp. for both ITO- and rGO-basedBPV devices. The highest difference occurred in ITO-based BPV device in light condition with a value of0.197 mW m−2 (157.6%). These could be attributed to theinternal structure such as the organization of thylakoidmembranes inside the S. elongatus which is less complexcompared to Chlorella sp. Charge separation in this simplethylakoid is directly exposed to the cytoplasm, increasingthe efficiency of electron transfer. Heterotrophic respirationin S. elongatus contributed to the high power output in darkcondition. The results obtained in this work demonstrate thepotential of local blue green microalgae strain as biomate-rials in BPV device for bioelectricity generation in bothlight and dark conditions.

References

Allahverdiyeva Y, Aro EM, Kosourov SN (2014) Recent developmentson cyanobacteria and green algae for biohydrogen photoproductionand its importance in CO2 reduction. In: Gupta V, Tuohy M,Kubicek CP, Saddler J, Xu F (eds) Bioenergy research: advancesand applications. Elsevier, New York, pp 367–387

Anderson SL,McIntosh L (1991) Light-activated heterotrophic growth ofthe cyanobacterium Synechocystis sp. strain PCC 6803: a blue-light-requiring process. J Bacteriol 173:2761–2767

Benemann JR (1997) Feasibility analysis of photobiological hydrogenproduction. Int J Hydrog Energy 22:979–987

Binder A (1982) Respiration and photosynthesis in energy-transducingmembranes of cyanobacteria. J Bioenerg Biomembr 14:271–286

Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, GhirardiM, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, MoserCC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, SayreRT (2011) Comparing photosynthetic and photovoltaic efficienciesand recognizing the potential for improvement. Science 332:805–809

Bombelli P, McCormick A, Bradley R, Yunus K, Philips J, Anderson X,Cruz S, Thorne R, Gu N, Smith A, Bendall D, Howe C, Peter L,Fisher A (2011) Harnessing solar energy by bio-photovoltaic (BPV)devices. Commun Agric Appl Biol Sci 76:89–91

Bradley RW, Bombelli P, Rowden SJL, Howe CJ (2012) Biological pho-tovoltaics: intra- and extra-cellular electron transport bycyanobacteria. Biochem Soc Trans 40:1302–1307

Chiao M, Lam KB, Lin L (2006) Micromachined microbial and photo-synthetic fuel cells. J Micromech Microeng 16:2547–2553

Furukawa Y, Moriuchi T, Morishima K (2005) Design principle andprototyping of direct photosynthetic/metabolic bio fuel cell(DPBFC). J Micromech Microeng 16:182–185

He Z, Kan J, Mansfeld F, Angenent LT, Nealson KH (2009) Self-sustained phototrophic microbial fuel cells based on the synergisticcooperation between photosynthetic microorganisms and heterotro-phic bacteria. Environ Sci Technol 43:1648–1654

Helmut A (2005) The economics of wind energy within the generationmix. Int J Energy Technol Policy 3:158–182

Hwang J, Amy F, Kahn A (2006) Spectroscopic study on sputteredPEDOT·PSS: role of surface PSS layer. Org Electron 7:387–396

Ibrahim SA, Jaafar MM, Ng FL, Phang SM, Kumar GG, Majid WHA,Periasamy V (2018) Plasma-treated Langmuir–Blodgett reducedgraphene oxide thin film for applications in biophotovoltaics. ApplPhys A 124:59

Jiang H, Luo S, Shi X, Dai M, Guo R (2012) A novel microbial fuel celland photobioreactor system for continuous domestic wastewatertreatment and bioelectricity generation. Biotechnol Lett 34:1269–1274

Khetkorn W, Rastogi RP, Incharoensakdi A, Lindblad P, Madamwar D,Pandey A, Larroche C (2017) Microalgal hydrogen production—areview. Bioresour Technol 243:1194–1206

Kim JY, Kim SH, Lee H, Lee K, MaW, Gong X, Heeger AJ (2006) Newarchitecture for high-efficiency polymer photovoltaic cells usingsolution-based titanium oxide as an optical spacer. Adv Mater 18:572–576

Kostarelos K, Novoselov KS (2014) Exploring the interface of grapheneand biology. Science 344:261–263

Lim SL, Chu WL, Phang SM (2010) Use of Chlorella vulgaris for bio-remediation of textile wastewater. Bioresour Technol 101:7314–7322

McCormickAJ, Bombelli P, Scott AM, Philips AJ, Smith AG, Fisher AC,Howe CJ (2011) Photosynthetic biofilms in pure culture harnesssolar energy in a mediatorless bio-photovoltaic cell (BPV) system.Energy Environ Sci 4:4699–4709

J Appl Phycol

Ng FL, Phang SM, Periasamy V, Yunus K, Fisher AC (2014a) Evaluationof algal biofilms on indium tin oxide (ITO) for use in biophotovoltaicplatforms based on photosynthetic performance. PLoS One 9:e97643

Ng FL, Jaafar MM, Phang SM, Chan Z, Salleh NA, Azmi SZ, Yunus K,Fisher AC, Periasamy V (2014b) Reduced graphene oxide anodesfor potential application in algae biophotovoltaic platforms. Sci Rep4:7562

Ng FL, Phang SM, Periasamy V, Yunus K, Fisher AC (2017)Enhancement of power output by using alginate immobilized algaein biophotovoltaic devices. Sci Rep 7:16237

Nishio K, Hashimoto K, Watanabe K (2010) Light/electricity conversionby a self-organized photosynthetic biofilm in a single-chamber re-actor. Appl Microbiol Biotech 86:957–964

Pelroy RA, Bassham JA (1972) Photosynthetic and dark carbon metab-olism in unicellular blue-green algae. Arch Microbiol 86:25–38

Phang SM, Chu WL (1999) Catalogue of Strains, University of MalayaAlgae Culture Collection (UMACC). Institute of PostgraduateStudies and Research, University of Malaya, Kuala Lumpur

Pisciotta JM, Zou Y, Baskakov IV (2010) Light-dependent electrogenicactivity of cyanobacteria. PLoS One 5:e10821

Prince RC, Kheshgi HS (2005) The photobiological production of hydro-gen: potential efficiency and effectiveness as a renewable fuel. CritRev Microbiol 31:19–31

Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R(2011) Renewable energy from cyanobacteria: energy productionoptimization by metabolic pathway engineering. Appl MicrobiolBiotechnol 91:471–490

Smith AJ (1982) Modes of cyanobacterial carbon metabolism. In: CarrNG, Whitton BA (eds) The biology of cyanobacteria. University ofCalifornia Press, Berkeley, pp 47–86

Strickland JDH, Parsons TRA (1968) Practical handbook of seawateranalysis. The Alger Press Lt., Ottawa

Strycharz-Glaven SM, Glaven RH,Wang Z, Zhou J, Vora GJ, Tender LM(2013) Electrochemical investigation of a microbial solar cell re-veals a nonphotosynthetic biocathode catalyst. Appl EnvironMicrobiol 79:3933–3942

Tamulonis C, Postma M, Kaandorp J (2011) Modeling filamentouscyanobacteria reveals the advantages of long and fast trichomesfor optimizing light exposure. PLoS One 6:e22084

Tanaka K, Tamamushi R, Ogawa T (1985) Bioelectrochemical fuel-cellsoperated by the cyanobacterium, Anabaena variabilis. J ChemTechnol Biotechnol 35:191–197

Yagishita T, Sawayama S, Tsukahara K, Ogi T (1997) Effects of intensityof incident light and concentrations of Synechococcus sp. and 2-hydroxy-1,4-naphthoquinone on the current output of photosynthet-ic electrochemical cell. Sol Energy 61:347–353

J Appl Phycol