Quantitative analysis of the factors limiting solar power transduction by Synechocystis sp. PCC 6803 in biological photovoltaic devices

Recent advances in fuel cell (FC) and microbial fuel cell (MFC) research have demonstrated these electrochemical technologies as effective methods for generating electrical power from chemical fuels and organic compounds. This led to the development of MFC-inspired photovoltaic (BPV) devices that produce electrical power by harvesting solar energy through biological activities of photosynthetic organisms. We describe the fabrication of a BPV device with multiple microchannels. This allows a direct comparison between sub-cellular photosynthetic organelles and whole cells, and quantitative analysis of the parameters affecting power output. Electron transfer within the photosynthetic materials was studied using the metabolic inhibitors DCMU (3-(3,4-dichlorophenyl)-1,1-dimethylurea) and methyl viologen (1,1′-dimethyl-4,4′-bipyridinium dichloride). These experiments suggest that the electrons that cause an increase in power upon illumination leave the photosynthetic electron transfer chain from the reducing end of photosystem I. Several key factors limiting performance efficiency, including density of the photosynthetic catalyst, electron carrier concentration, and light intensity were investigated.

[1]  T. Donohue,et al.  Development of a solar‐powered microbial fuel cell , 2008, Journal of applied microbiology.

[2]  R. J. Porra,et al.  Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy , 1989 .

[3]  Christopher J. Howe,et al.  Photosynthetic biofilms in pure culture harness solar energy in a mediatorless bio-photovoltaic cell (BPV) system† , 2011 .

[4]  R. Berk,et al.  BIOELECTROCHEMICAL ENERGY CONVERSION. , 1964, Applied microbiology.

[5]  Tina L. M. Derzaph,et al.  Iron limitation results in induction of ferricyanide reductase and ferric chelate reductase activities in Chlamydomonas reinhardtii , 1998, Planta.

[6]  K. Satoh,et al.  Binding affinities of benzoquinones to the QB site of Photosystem II in Synechococcus oxygen-evolving preparation , 1992 .

[7]  John M. Pisciotta,et al.  Light-Dependent Electrogenic Activity of Cyanobacteria , 2010, PloS one.

[8]  Peng Liang,et al.  A completely anoxic microbial fuel cell using a photo-biocathode for cathodic carbon dioxide reduction , 2009 .

[9]  V. De Pinto,et al.  VDAC1 Is a Transplasma Membrane NADH-Ferricyanide Reductase* , 2004, Journal of Biological Chemistry.

[10]  Zhen He,et al.  Self-sustained phototrophic microbial fuel cells based on the synergistic cooperation between photosynthetic microorganisms and heterotrophic bacteria. , 2009, Environmental science & technology.

[11]  Kevin E. Healy,et al.  Bioelectrocatalytic self-assembled thylakoids for micro-power and sensing applications , 2006 .

[12]  Alice Dohnalkova,et al.  Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Hubertus V. M. Hamelers,et al.  Green electricity production with living plants and bacteria in a fuel cell , 2008 .

[14]  Peter Roepstorff,et al.  Central Functions of the Lumenal and Peripheral Thylakoid Proteome of Arabidopsis Determined by Experimentation and Genome-Wide Prediction Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010304. , 2002, The Plant Cell Online.

[15]  A. Glazer,et al.  Characterization of a cyanobacterial photosystem I complex. , 1985, The Journal of biological chemistry.

[16]  Kenji Kano,et al.  Photosynthetic bioelectrochemical cell utilizing cyanobacteria and water-generating oxidase , 2001 .

[17]  P. Rich,et al.  THE INTERACTIONS OF DUROQUINOL, DBMIB AND NQNO WITH THE CHLOROPLAST CYTOCHROME BF COMPLEX , 1991 .

[18]  Uwe Schröder,et al.  In situ electrooxidation of photobiological hydrogen in a photobioelectrochemical fuel cell based on Rhodobacter sphaeroides. , 2005, Environmental science & technology.

[19]  Derek R. Lovley,et al.  Bug juice: harvesting electricity with microorganisms , 2006, Nature Reviews Microbiology.

[20]  W. Oettmeier,et al.  Competition between plastoquinone and 3-(3,4-dichlorophenyl)-1,1-dimethylurea at the acceptor side of photosystem II , 1983 .

[21]  Hubertus V. M. Hamelers,et al.  Renewable sustainable biocatalyzed electricity production in a photosynthetic algal microbial fuel cell (PAMFC) , 2008, Applied Microbiology and Biotechnology.

[22]  L. T. Angenent,et al.  Light energy to bioelectricity: photosynthetic microbial fuel cells. , 2010, Current opinion in biotechnology.

[23]  Kevin J. Emmett,et al.  Photosystem I - based biohybrid photoelectrochemical cells. , 2010, Bioresource technology.

[24]  J. Barber,et al.  Novel effects of methyl viologen on photosystem II function in spinach leaves , 2009, European Biophysics Journal.

[25]  P. Liang,et al.  Electricity generation by an enriched phototrophic consortium in a microbial fuel cell , 2008 .

[26]  Uwe Schröder,et al.  Utilizing the green alga Chlamydomonas reinhardtii for microbial electricity generation: a living solar cell , 2005, Applied Microbiology and Biotechnology.

[27]  D. Lowy,et al.  A self-assembling self-repairing microbial photoelectrochemical solar cell , 2009 .

[28]  Y. Amao,et al.  Bio-photovoltaic conversion device using chlorine-e6 derived from chlorophyll from Spirulina adsorbed on a nanocrystalline TiO2 film electrode. , 2004, Biosensors & bioelectronics.

[29]  R. Chow,et al.  A microelectrochemical technique to measure trans‐plasma membrane electron transport in plant tissue and cells in vivo , 2001 .

[30]  R. Pilloton,et al.  Direct mediatorless electron transport between the monolayer of photosystem II and poly(mercapto-p-benzoquinone) modified gold electrode--new design of biosensor for herbicide detection. , 2005, Biosensors & bioelectronics.

[31]  B. Logan Exoelectrogenic bacteria that power microbial fuel cells , 2009, Nature Reviews Microbiology.

[32]  Robert Eugene Blankenship,et al.  Light saturation curves and quantum yields in reaction centers from photosynthetic bacteria. , 1984, Biophysical journal.

[33]  E. Hall,et al.  DIAMINODURENE AS A MEDIATOR OF A PHOTOCURRENT USING INTACT CELLS OF CYANOBACTERIA , 1994 .

[34]  John M. Pisciotta,et al.  Photosynthetic microbial fuel cells with positive light response , 2009, Biotechnology and bioengineering.

[35]  J. Appel,et al.  Localization of cytochrome b6f complexes implies an incomplete respiratory chain in cytoplasmic membranes of the cyanobacterium Synechocystis sp. PCC 6803. , 2009, Biochimica et biophysica acta.

[36]  W. Verstraete,et al.  Microbial fuel cells generating electricity from rhizodeposits of rice plants. , 2008, Environmental science & technology.

[37]  Tibor Fabian,et al.  Direct extraction of photosynthetic electrons from single algal cells by nanoprobing system. , 2010, Nano letters.

[38]  M. Chiao,et al.  A MEMS Photosynthetic Electrochemical Cell Powered by Subcellular Plant Photosystems , 2006, Journal of Microelectromechanical Systems.

[39]  David E Cliffel,et al.  Functionalized nanoporous gold leaf electrode films for the immobilization of photosystem I. , 2008, ACS nano.

[40]  R. Geider,et al.  PHYTOPLANKTON PLASMA MEMBRANE REDOX ACTIVITY: EFFECT OF IRON LIMITATION AND INTERACTION WITH PHOTOSYNTHESIS 1 , 2003 .

[41]  Zhen He,et al.  Effects of anolyte recirculation rates and catholytes on electricity generation in a litre-scale upflow microbial fuel cell , 2010 .

[42]  Wolfgang Schuhmann,et al.  Photo‐Induced Electron Transfer Between Photosystem 2 via Cross‐linked Redox Hydrogels , 2008 .

[43]  Artificial quenchers of chlorophyll fluorescence do not protect against photoinhibition , 1999 .

[44]  M. Medina,et al.  Effects of photoacclimation on plasma membrane ferricyanide reductase from the rhodophyta Gracilaria tenuistipitata , 2002 .

[45]  M. Bowman,et al.  The inhibitor DBMIB provides insight into the functional architecture of the Qo site in the cytochrome b6f complex. , 2004, Biochemistry.

[46]  Kazuya Watanabe,et al.  Plant/microbe cooperation for electricity generation in a rice paddy field , 2008, Applied Microbiology and Biotechnology.

[47]  Kenji Kano,et al.  Electrochemical investigation of cyanobacteria Synechococcus sp. PCC7942-catalyzed photoreduction of exogenous quinones and photoelectrochemical oxidation of water , 2001 .