Engineering natural photosynthesis

Huub J. M. de Groot

doi:10.1017/CBO9780511718786.032

28 - Engineering natural photosynthesis

from Part 3 - Renewable energy sources

Published online by Cambridge University Press: 05 June 2012

Huub J. M. de Groot

Edited by

David S. Ginley and

David Cahen

Show author details

Huub J. M. de Groot: Affiliation:
Leiden Institute of Chemistry, Leiden University, Leiden, the Netherlands
David S. Ginley: Affiliation:
National Renewable Energy Laboratory, Colorado
David Cahen: Affiliation:
Weizmann Institute of Science, Israel

Book contents

Get access

Summary

Focus

What is called in this chapter the “engineering” of natural photosynthesis has been performed by evolution over several billions of years. Its optimization, against thermodynamic and other selection criteria from the biological environment, has led to a remarkably limited set of molecular and supramolecular motifs. Photosynthesis starts with absorption of light by mutually interacting chlorophyll (Chl) and related molecules. These are embedded in protein matrices that promote rapid transport of energy by excitons and lower the energy of transition states for charge separation and multielectron catalysis. An understanding of engineered natural photosynthesis is the underpinning of the design of artificial solar-to-fuel devices.

Synopsis

Light energy is abundant and evenly spread over the surface of the Earth, and virtually all organisms depend on the conversion and chemical storage of light energy by natural photosynthesis. The advent of natural photosynthesis opened up new energy conversion pathways for progression toward thermodynamic equilibrium between the very hot Sun and the much colder Earth. The first-principles thermodynamic and mechanistic analysis of how natural photosynthesis is engineered by biological evolution in this chapter shows that combining different functionalities of light harvesting, charge separation, and catalysis in small molecules or at a single narrow interface is incompatible with high solar-to-fuel conversion efficiency, and that possible solutions to the problem of accumulation of solar energy in chemicals require complex device topologies. This led biology to a modular design approach that is the basis of photosynthesis. It is the result of an intensive evolutionary effort of shaping complex structures, driven by the abundant solar energy spread over the planet.

Type: Chapter
Information: Fundamentals of Materials for Energy and Environmental Sustainability , pp. 365 - 378

DOI: https://doi.org/10.1017/CBO9780511718786.032 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Giacometti, G.Giacometti, G. M. 2010 “Evolution of photosynthesis and respiration: which came first?,”Appl. Magn. Reson. 37 13CrossRef Google Scholar

Falkowski, P. G.Knoll, A. H. 2007 Evolution of Primary Producers in the SeaSan Diego, CAAcademic Press

Duysens, L. N. M.Amesz, J.Kamp, B. M. 1961 “Two photochemical systems in photosynthesis,”Nature 190 510CrossRef Google Scholar

Grotjohann, I.Jolley, C.Fromme, P. 2004 “Evolution of photosynthesis and oxygen evolution: implications from the structural comparison of Photosystems I and II,”Phys. Chem. Chem. Phys. 6 4743CrossRef Google Scholar

Prince, R. C.Kheshgi, H. S. 2005 “The photobiological production of hydrogen: potential efficiency and effectiveness as a renewable fuel,”Crit. Rev. Microbiol. 31 19CrossRef Google Scholar

Blankenship, R. E. 2002 Molecular Mechanisms of PhotosynthesisOxfordBlackwell ScienceCrossRef Google Scholar

Fromme, P.Jordan, P.Krauss, N. 2001 “Structure of photosystem I,”Biochim. Biophys. Acta – Bioenergetics 1507 5CrossRef Google Scholar

Ferreira, K. N.Iverson, T. M.Maghlaoui, K.Barber, J.Iwata, S. 2004 “Architecture of the photosynthetic oxygen-evolving center,”Science 303 1831CrossRef Google Scholar

Yoder, L. M.Cole, A. G.Sension, R. J. 2002 “Structure and function in the isolated reaction center complex of photosystem II: energy and charge transfer dynamics and mechanism,”Photosynthesis Res. 72 147CrossRef Google Scholar

Hunter, C. N. 2009 The Purple Phototrophic BacteriaDordrechtSpringerCrossRef Google Scholar

Sener, M. K.Olsen, J. D.Hunter, C. N.Schulten, K. 2007 “Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle,”Proc. Natl. Acad. Sci. 104 15723CrossRef Google Scholar

Ganapathy, S.Oostergetel, G. T.Wawrzyniak, P. K. 2009 “Alternating syn–anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes,”Proc. Natl. Acad. Sci. 106 8525CrossRef Google Scholar

Li, Y. F.Zhou, W. L.Blankenship, R. E.Allen, J. P. 1997 “Crystal structure of the bacteriochlorophyll protein from ,”J. Mol. Biol. 271 456CrossRef Google Scholar

MacColl, R. 1998 “Cyanobacterial phycobilisomes,”J. Struct. Biol. 124 311CrossRef Google Scholar

Shockley, W.Queisser, H. J. 1961 “Detailed balance limit of efficiency of p–n junction solar cells,”J. Appl. Phys. 32 510CrossRef Google Scholar

Hanna, M. C.Nozik, A. J. 2006 “Solar conversion efficiency of photovoltaic and photoelectrolysis cells with carrier multiplication absorbers,”J. Appl. Phys. 100 074510CrossRef Google Scholar

Ross, R. T.Calvin, M. 1967 “Thermodynamics of light emission and free-energy storage in photosynthesis,”Biophys. J. 7 595CrossRef Google Scholar

Markvart, T.Landsberg, P. 2002 “Thermodynamics and reciprocity of solar energy conversion,”Physica E 14 71CrossRef Google Scholar

de Groot, H. J. M. 2010 “Integration of catalysis with storage for the design of multi-electron photochemistry devices for solar fuel,”Appl. Magn. Reson. 37 497CrossRef Google Scholar

van Gorkom, H. J. 1986 “Photochemistry of photosynthetic reaction centres,”Bioelectrochem. Bioenergetics 16 77CrossRef Google Scholar

Noy, D.Moser, C. C.Dutton, P. L. 2006 “Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales,”Biochim. Biophys. Acta 1757 90CrossRef Google Scholar

Janssen, M.Tramper, J.Mur, L. R.Wijffels, R. H. 2003 “Enclosed outdoor photobioreactors: light regime, photosynthetic efficiency, scale-up, and future prospects,”Biotechnol. Bioeng. 81 193CrossRef Google Scholar

Bahatyrova, S.Frese, R. N.Siebert, C. A. 2004 “The native architecture of a photosynthetic membrane,”Nature 430 1058CrossRef Google Scholar

Shelnutt, J. A.Song, X.-Z.Ma, J.-G. 2010

Pandit, A.Buda, F.van Gammeren, A. J.Ganapathy, S.De Groot, H. J. M. 2010 “Selective chemical shift assignment of bacteriochlorophyll in uniformly [13C–15N]-labeled light-harvesting 1 complexes by solid-state NMR in ultrahigh magnetic field,”J. Phys. Chem. B 114 6207CrossRef Google Scholar

Pandit, A.Wawrzyniak, P. K.van Gammeren, A. J. 2010 “Nuclear magnetic resonance secondary shifts of a light-harvesting 2 complex reveal local backbone perturbations induced by its higher-order interactions,”Biochemistry 49 478CrossRef Google Scholar

van Grondelle, R.Novoderezhkin, V. I. 2006 “Energy transfer in photosynthesis: experimental insights and quantitative models,”Phys. Chem. Chem. Phys. 8 793CrossRef Google Scholar

Wawrzyniak, P. K.Alia, A.Schaap, R. G. 2008 “Protein-induced geometric constraints and charge transfer in bacteriochlorophyll–histidine complexes in LH2,”Phys. Chem. Chem. Phys. 10 6971CrossRef Google Scholar

van Grondelle, R.Dekker, J. P.Gillbro, T.Sundstrom, V. 1994 “Energy-transfer and trapping in photosynthesis,”Biochim. Biophys. Acta – Bioenergetics 1187 1CrossRef Google Scholar

Liu, Z.Yan, H.Wang, K. 2004 “Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution,”Nature 428 287CrossRef Google Scholar

Robert, B.Horton, P.Pascal, A. A.Ruban, A. V. 2004 “Insights into the molecular dynamics of plant light-harvesting proteins ,”Trends Plant Sci. 9 385CrossRef Google Scholar

Müller, M. G.Lambrev, P.Reus, M. 2010 “Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids,”ChemPhySchem 11 1289CrossRef Google Scholar

Ruban, A. V.Berera, R.Ilioaia, C. 2007 “Identification of a mechanism of photoprotective energy dissipation in higher plants,”Nature 450 575CrossRef Google Scholar

Ahn, T. K.Avenson, T. J.Ballottari, M. 2008 “Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein,”Science 320 794CrossRef Google Scholar

Förster, T. 1965 “Delocalized excitation and excitation transfer,”Modern Quantum ChemistrySinanoğlu, O.New YorkAcademic Press93Google Scholar

Prokhorenko, V. I.Steensgaard, D. B.Holzwarth, A. R. 2003 “Exciton theory for supramolecular chlorosomal aggregates: 1. Aggregate size dependence of the linear spectra,”Biophys. J. 85 3173CrossRef Google Scholar

Golbeck, J. H. 2003

Marcus, R. A. 1956 “On the theory of oxidation–reduction reactions involving electron transfer. 1J. Chem. Phys. 24 966CrossRef Google Scholar

Moser, C. C.Keske, J. M.Warncke, K.Farid, R. S.Dutton, P. L. 1992 “Nature of biological electron transfer,”Nature 355 796CrossRef Google Scholar

Closs, G. L.Miller, J. R. 1988 “Intramolecular long-distance electron transfer in organic molecules,”Science 240 440CrossRef Google Scholar

Reece, S. Y.Nocera, D. G. 2009 “Proton-coupled electron transfer in biology: results from synergistic studies in natural and model systems,”Ann. Rev. Biochem. 78 673CrossRef Google Scholar

Haumann, M.Liebisch, P.Müller, C. 2005 “Photosynthetic O2 formation tracked by time-resolved X-ray experiments,”Science 310 1019CrossRef Google Scholar

Dau, H.Zaharieva, I. 2009 “Principles, efficiency, and blueprint character of solar-energy conversion in photosynthetic water oxidation,”Acc. Chem. Res. 42 1861CrossRef Google Scholar

Book contents

28 - Engineering natural photosynthesis

Summary

Access options

References

Save book to Kindle

Save book to Dropbox

Save book to Google Drive