Photoelectrochemical cells based on photosynthetic systems: a review

Document Type : Review Paper

Authors

1 Controlled Photobiosynthesis Laboratory, Institute of Plant Physiology, Russian Academy of Sciences, Moscow 127276, Russia.

2 Institute of Basic Biological Problems, Russian Academy of Sciences, Moscow 142290, Russia.

3 Center for Nanofibers and Nanotechnology, Department of Mechanical Engineering, National University of Singapore, 117576, Singapore.

4 Department of Plant Physiology, Faculty of Biology, M.V. Lomonosov Moscow State University, Moscow 119991, Russia.

Abstract

Photosynthesis is a process which converts light energy into energy contained in the chemical bonds of organic compounds by photosynthetic pigments such as chlorophyll (Chl a, b, c, d, f) or bacteriochlorophyll. It occurs in phototrophic organisms, which include higher plants and many types of photosynthetic bacteria, including cyanobacteria. In the case of the oxygenic photosynthesis, water is a donor of both electrons and protons, and solar radiation serves as inexhaustible source of energy. Efficiency of energy conversion in the primary processes of photosynthesis is close to 100%. Therefore, for many years photosynthesis has attracted the attention of researchers and designers looking for alternative energy systems as one of the most efficient and eco-friendly pathways of energy conversion. The latest advances in the design of optimal solar cells include the creation of converters based on thylakoid membranes, photosystems, and whole cells of cyanobacteria immobilized on nanostructured electrode (gold nanoparticles, carbon nanotubes, nanoparticles of ZnO and TiO2). The mode of solar energy conversion in photosynthesis has a great potential as a source of renewable energy while it is sustainable and environmentally safety as well. Application of pigments such as Chl f and Chl d (unlike Chl a and Chl b), by absorbing the far red and near infrared region of the spectrum (in the range 700-750 nm), will allow to increase the efficiency of such light transforming systems. This review article presents the last achievements in the field of energy photoconverters based on photosynthetic systems.

Graphical Abstract

Photoelectrochemical cells based on photosynthetic systems: a review

Keywords


Klimov, V.V., Mimuro, M., 2010. Redox potential of pheophytin a in photosystem II of two cyanobacteria having the different special pair chlorophylls. Proc. Natl. Acad Sci. USA. 107(8), 3924-3929.
Andralojc, J., Harris, D.A., 1992. The chloroplast ATP-synthase — a light regulated enzyme. Biochem. Educ.  20(1), 44-48.
Badura, A., Guschin, D.,  Esper, B.,  Kothe, T., Neugebauer, S., Schuhmann, W.,  Rogner, M., 2008. Photo-induced electron transfer between  photosystem  2  via crosslinked redox hydrogels. Electroanalysis. 20, 1043-1047.
Bedford, N.M., Winget, G.D., Punnamaraju, S., Steckl, A.J., 2011. Immobilization of stable thylakoid  vesicles  in  conductive  nanofibers  by  electrospinning. Biomacromolecules.  12(3), 778-784.
Blankenship, R.E., 2002. Molecular Mechanisms of Photosynthesis. Blackwell Science, Oxford.
Blankenship, R.E., 2010. Early Evolution of Photosynthesis. Plant Physiol.154, 434-438.
Blankenship, R.E., Chen, M., 2013. Spectral expansion and antenna reduction can enhance photosynthesis for energy production. Current Opinion in Chem. Biol. 17, 457-461.
Blankenship, R.E., Hartman, H., 1998. The origin and evolution of oxygenic photosynthesis. Trends Biochem. Sci. 23, 94-97.
Blankenship, R.E.,  Tiede, D.M., Barber, J., Brudvig, G.W., Fleming, G., Ghirardi, M.R., Gunner, M., Junge, W., Kramer, D.M.,  Melis, A., Moore, T.A.,  Moser, C.C., Nocera, D.G.,  Nozik, A.J., Ort, D.R., Parson, W.W., Prince, R.C., Sayre, R.T., 2011. Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement, Science. 332, 805-809.
Bryant, D. B. (Ed.) 1994. The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, Boston.
Calkins, J.O., Umasankar, Y., O’Neill, H., Ramasamy, R.P., 2013. High photoelectrochemical activity  of thylakoid-carbon nanotube composites for  photosynthetic energy conversion. Energy Environ. Sci. 6, 1891-1900.
Carpentier, R., Lemieux, S., Mimeault, M., Purcell, M., Goetze, D.C., 1999. A photoelectrochemical cell using immobilized photosynthetic membranes. Bioelectrochem.  Bioenerg.  22, 391-401.
Chen, M., Blankenship, R.E., 2011. Expanding the solar spectrum used by photosynthesis. Trends Plant Sci. 16, 427-431.
Chen, M., Scheer, H., 2013. Extending the limit of natural photosynthesis and implications of technical light harvesting.  J. Porphyrins Phthalocyanines. 17, 1-15.
Chen, M., Schliep, M., Willows, R.D., Cai, Z.-L., Neilan, B.A., Scheer, H., 2010. A red-shifted chlorophyll. Science. 329, 1318-1319.
Ciesielski, P.N., Hijazi, F.M., Scott, A.M., Faulkner, C.J., Beard, L., Emmett, K., Rosenthal, S.J., Cliffel, D., Jennings, G.K., 2010. Photosystem I – Based biohybrid photoelectrochemical cells. Bioresour. Technol. 101, 3047-3053.
Das, R., 2004. Photovoltaic devices using photosynthetic protein complexes. Doctoral dissertation. Ph.D. thesis, Massachusetts Institute of Technology, Boston.
Das, R., Kiley, P.J., Segal, M., Norville, J., Yu, A.A., Wang, L.Y., Trammell, S.A., Reddick, L.E.,  Kumar, R.,  Stellacci, F., Lebedev, N., Schnur, J., Bruce, B.D., Zhang, S.G., Baldo, M., 2004. Integration of Photosynthetic Protein Molecular Complexes in Solid-State Electronic Devices. Nano Lett. 4, 1079-1083.
Faulkner, C.J., Lees, S., Ciesielski, P.N., Cliffel, D.E., Jennings, G.K., 2008. Rapid  assembly  of  photosystem  I  monolayers  on  gold  electrodes.  Langmuir.  24, 8409-8412.
Fourmond, V.,  Lagoutte, B., Setif, P.,  Leibl, W.,  Demaille, C., 2007.  Electrochemical  study of  a  reconstituted  photosynthetic  electron-transfer  chain.  J. Am. Chem. Soc. 129, 9201-9209.
Frolov, L., Wilner, O., Carmeli, C., Carmeli, I., 2008. Fabrication of oriented multilayers of photosystem I proteins on solid surfaces by auto-metallization. Adv. Mater. 20, 263-266.
Fujishima, A., Honda, K., 1972. Electrochemical  photolysis  of  water  at  a  semiconductor  electrode. Nature.  238, 37-38.
Fultz, M.L., Durst, R.A., 1982. Mediator compounds  for  the  electrochemical  study  of biological redox  systems – a compilation. Anal. Chim.  Acta.  140, 1-18.
Furukawa,Y., Moriuchi, T., Morishima, K., 2006.Design principle and prototyping of a direct photosynthetic/metabolic biofuel cell  (DPMFC). J.  Micromech.  Microeng.  16, 220-225.
Grätzel, M.,  2001. Photoelectrochemical cells. Nature. 414, 338-344.
Grätzel, M., 2007. Photovoltaic and photoelectrochemical conversion of solar energy. Phil. Trans. R. Soc. 365, 993-1005.
Goldsmith, J.O., Boxer, S.G., 1996.  Rapid  isolation  of  bacterial  photosynthetic  reaction  centers  with  an  engineered  poly-histidine  tag.  Biochim. Biophys. Acta, Bioenerg. 1276, 171-175.
Hanna, M.C.,  Nozik, A.J., 2006. Solar conversion efficiency of  photovoltaic and photoelectrolysis cells  with carrier multiplication absorbers. J. Appl. Phys. 100, 1-8.
Iengo, E., Zangrando, E., Alessio, E., 2003. Discrete supramolecular assemblies of porphyrins mediated by coordination compounds. Eur. J. Inorg. Chem. 2003, 2371-2384.
Iwuchukwu, I.J., Vaughn, M., Myers, N., O’Neill, H., Frymier, P., Bruce, B.D., 2010. Selforganized  photosynthetic nanoparticle for cell-free hydrogen  prod. Nat. Nanotechnol. 5, 73-79.
Kincaid, H.A., Niedringhaus, T., Ciobanu, M., Cliffel, D.E., Jennings, G.K., 2006. Entrapment of  photosystem I within self-assembled  films.  Langmuir.  22, 8114-8120.
Krassen, H., Ott, S., Heberle, J., 2011.  In vitro hydrogen production – using energy fromthe sun. Phys. Chem. Chem. Phys. 13, 47-57.
Larom, S.,  Salama, F.,  Schuster, G., Adir, N., 2010. Engineering of an alternative electron transfer path in photosystem II. Proc. Natl. Acad. Sci. U.S.A. 107, 9650-9655.
Loughlin, P., Lin, Y., Chen, M., 2013. Chlorophyll d and Acaryochloris marina: current status. Photosynth. Res. 116(2-3), 277-293.
Marshall, J., 2014. Solar energy: Springtime for the artificial leaf. Nature. 510, 22-24.
Mershin, A., Matsumoto, K., Kaiser, L., Yu, D.Y., Vaughn, M., Nazeeruddin, M.K., Bruce, B.D., Graetzel, M., Zhang, S.G., 2012. Self-assembled  photosystem-I  biophotovoltaics  on  nanostructured  TiO2 and  ZnO.  Sci.  Rep.  2, 1-7.
Meunier, C.F., Van Cutsem, P., Kwon, Y.U., Su, B.L., 2009. Thylakoids entrapped within porous silica gel: towards living matter able to convert energy. J. Mater. Chem. 19, 1535-1542.
Nakamura, C., Hasegawa, M., Yasuda, Y., Miyake, J., 2000. Self-assembling photosynthetic reaction  enters on electrodes for current generation. Appl.  Biochem. Biotechnol. 84(6), 401-408.
Nelson, N., Yocum, C.F., 2006. Structure and function of photosystem I and II. Annu. Rev. Plant Biol. 57, 521-565.
Noji, T., Suzuki, H., Gotoh, T., Iwai, M., Ikeuchi, M., Tomo, T., Noguchi, T., 2011. Photosystem II-gold  nanoparticle conjugate as  a nanodevice for the  development of  artificial  light-driven water-splitting systems. J. Phys. Chem. Lett. 2, 2448-2452.
Pisciotta,J.M., Zou, Y., Baskakov, I.V., 2010. Light-dependent electrogenic activity of cyanobacteria. PLoS ONE. 5(5), 1-10.
Sanders, J.K.M., 2000. Porphyrin Handbook. Academic Press, New York, USA.
Sandman, G., 2009. Evolution of carotenoid desaturation: the complication of a simple pathway. Arch. Biochem Biophys. 483,169-174.
Scheer, H., 2006. An overview of chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications, in: Grimm, B., Porra, R.J., Rüdiger, W., Scheer, H. (Eds.) Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications, Springer, Dordrecht, pp. 4-11.
Sekar, N., Ramasamy, R.P., 2015. Recent advances in photosynthetic energy conversion. J. Photochem. Photobiol., C. 22, 19-33.
Sekar, N., Umasankar, Y., Ramasamy, R.P., 2014.  Photocurrent  generation  by  immobilized  cyanobacteria  via  direct  electron  transport  in  photo-bioelectrochemical cells. Phys. Chem. Chem. Phys.16(17), 7862-7871.
Tomo, T., Akimoto, S., Tsuchiya, T., Fukuya, M., Tanaka, K., Mimuro, M., 2008. Isolation and spectral characterization of Photosystem II reaction center from Synechocystis sp. PCC 6803. Photosynth. Res.98, 293-302.
Tomo, T., Shinoda, T., Chen, M., Allakhverdiev, S.I., Akimoto, S., 2014. Energy transfer processes in chlorophyll f-containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells. Biochim. Biophys. Acta.1837, 1484-1489.
Torimura, M., Miki, A., Wadano, A., Kano, K., Ikeda, T., 2001. Electrochemical investigation of cyanobacteria Synechococcus sp. PCC7942-catalyzed  photoreduction of exogenous quinones and photoelectrochemical oxidation of water. J. Electroanal. Chem. 496, 21-28.
Vittadello, M., Gorbunov, M.Y., Mastrogiovanni, D.T., Wielunski, L.S.,  Garfunkel, E.L., Guerrero, F., Kirilovsky, D., Sugiura, M., Rutherford, A.W.,  Safari, A., Falkowski, P.G., 2010. Photoelectron generation by photosystem II core complexes tethered to gold surfaces. ChemSusChem. 3, 471-475.
Ulas, G., Brudvig, G.W., 2011. Redirecting electron transfer in  photosystem II from water to redox-active metal complexes. J. Am. Chem. Soc. 133, 13260-13263.
Whitney, S.M., Houtz, R.L., Alonso, H., 2011. Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol. 155, 27-35.
Yagishita, T., Horigome, T., Tanaka, K., 1993. Effects of light, CO2 and inhibitors on the current output of biofuel cells containing the photosynthetic organism Synechococcus sp. J. Chem. Technol. Biotechnol. 56, 393-399. 
Yehezkeli, O., Tel-Vered, R., Wasserman, J., Trifonov, A., Michaeli, D., Nechushtai, R., Willner, I., 2012. Integrated photosystem II-based photo-bioelectrochemical cells. Nat. Commun. 3,742, 1-7.