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Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms † ‡ § ∥ ⊥ Tihana Mirkovic, Evgeny E

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Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms † ‡ § ∥ ⊥ Tihana Mirkovic, Evgeny E Review pubs.acs.org/CR Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms † ‡ § ∥ ⊥ Tihana Mirkovic, Evgeny E. Ostroumov, Jessica M. Anna, Rienk van Grondelle, Govindjee, † ‡ and Gregory D. Scholes*, , † Department of Chemistry, University of Toronto, 80 St. George Street, Toronto, Ontario M5S 3H6, Canada ‡ Department of Chemistry, Princeton University, Washington Road, Princeton, New Jersey 08544, United States § Department of Chemistry, University of Pennsylvania, 231 S. 34th Street, Philadelphia, Pennsylvania 19104, United States ∥ Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV, Amsterdam, The Netherlands ⊥ Department of Biochemistry, Center of Biophysics & Quantitative Biology, and Department of Plant Biology, University of Illinois at Urbana−Champaign, 265 Morrill Hall, 505 South Goodwin Avenue, Urbana, Illinois 61801, United States ABSTRACT: The process of photosynthesis is initiated by the capture of sunlight by a network of light-absorbing molecules (chromophores), which are also responsible for the subsequent funneling of the excitation energy to the reaction centers. Through evolution, genetic drift, and speciation, photosynthetic organisms have discovered many solutions for light harvesting. In this review, we describe the underlying photophysical principles by which this energy is absorbed, as well as the mechanisms of electronic excitation energy transfer (EET). First, optical properties of the individual pigment chromophores present in light-harvesting antenna complexes are introduced, and then we examine the collective behavior of pigment−pigment and pigment−protein interactions. The description of energy transfer, in particular multichromophoric antenna structures, is shown to vary depending on the spatial and energetic landscape, which dictates the relative coupling strength between constituent pigment molecules. In the latter half of the article, we focus on the light- harvesting complexes of purple bacteria as a model to illustrate the present understanding of the synergetic effects leading to EET optimization of light-harvesting antenna systems while exploring the structure and function of the integral chromophores. We end this review with a brief overview of the energy-transfer dynamics and pathways in the light-harvesting antennas of various photosynthetic organisms. CONTENTS 11.2. LH2 Model: Disorder and Exciton Delocal- ization AA 1. Introduction B 12. Energy-Transfer Time Scales AB 2. Spectral Composition of Light and the Pigments D ffi 12.1. LH2 of Purple Bacteria AB 3. Light-Harvesting Systems and Their E ciency F 12.2. LHCII of Higher Plants AC 4. Physical Principles of Antenna Architecture G 12.3. FCP and PCP of Brown and Dinoflagellate 5. Mechanism of Förster Excitation Energy Transfer J ̈ Algae AD 6. Beyond Forster Theory of Excitation Energy 12.4. Chlorosomes of Green Sulfur Bacteria AE Transfer M 12.5. Phycobilisomes of Cyanobacteria AE 6.1. Electronic Coupling and Orbital Overlap M 12.6. Phycobiliproteins of Cryptophyte Algae AE 6.2. Breakdown of the Dipole Approximation N 13. Carotenoids and Photoprotection AF 6.3. Solvent Screening N 14. Trapping of Energy AG 7. Molecular Excitons Q 15. Concluding Remarks AH 8. Structural and Spectral Considerations S ̈ Author Information AH 9. Excitonics and Generalized Forster Theory (GFT) S Corresponding Author AH 9.1. Excitons and Electronic Couplings U Notes AH 9.2. Formulating GFT V Biographies AH 10. Structure and Photophysics of Light-Harvesting Acknowledgments AI Complexes of Purple Bacteria V References AI 11. Structure and Absorption of Light-Harvesting Complexes X 11.1. LH2 Model: Electronic Coupling and Ex- Special Issue: Light Harvesting cition Formation Y Received: January 8, 2016 © XXXX American Chemical Society A DOI: 10.1021/acs.chemrev.6b00002 Chem. Rev. XXXX, XXX, XXX−XXX Chemical Reviews Review Scheme 1. (Top) Fine Tuning of the Function of a Light-Harvesting Apparatus Occurs through Photophysical Properties of Its Constituent Chromophores and Synergetic Effects Resulting from Their Collective Interactions and (Bottom) the Light- Harvesting Complexes of Purple Bacteria Illustrate Phenomena Affecting Excitation Energy Transfer 1. INTRODUCTION In the past century, curiosity-driven research led to the The development, nourishment, and regulation of all forms of discovery of the intricate structural and functional organization life on our planet are directed by sunlight. Photosynthesis, the of the photosynthetic apparatus, which has more recently also most important light-induced process, allows plants, algae, been fueled by the opportunity to mimic these natural cyanobacteria, and anoxygenic photosynthetic bacteria to processes in man-made energy-harvesting systems. A number fi convert energy harvested from light into a chemical form.1,2 of reviews have discussed the development of arti cial systems It is initiated by a sequence of remarkable and finely tuned based on molecular and supramolecular architectures, and photophysical and photochemical reactions (see Scheme 1, prospective redesigns of photosynthetic plant systems on top). The process of photosynthesis, which takes place over a various scales have been presented as plausible solutions to 5−11 hierarchy of time scales and distances, ultimately powers, global food and bioenergy demands. We have exciting days directly or indirectly, all living cells on the planet.3 Planet Earth ahead. reflects 30% of the incident 166 PW (1 PW = 1015 W) of solar There are two types of photosynthesis: oxygenic photosyn- power back into space; 19% is absorbed by the clouds, leaving thesis and anoxygenic photosynthesis. Plants, algae, and 85 PW available for terrestrial energy harvesting. Of this 85 PW cyanobacteria carry out oxygenic photosynthesis, whereby of solar radiation, only a small fraction, 75 TW (1 TW = 1012 carbon dioxide is reduced to carbohydrate and the oxidation W), is utilized for products of terrestrial photosynthesis or the of water delivers the necessary electrons and eventually leads to net global primary production through photosynthesis.4 To put oxygen production.12 However, in bacteria, other than these numbers in perspective, the average total power cyanobacteria, water is not used as the primary electron consumption of the human world in 2010 was 16 TW. donor, and no oxygen is produced during anoxygenic B DOI: 10.1021/acs.chemrev.6b00002 Chem. Rev. XXXX, XXX, XXX−XXX Chemical Reviews Review Figure 1. (a) Spectral distributions of sunlight that reaches the top and base of a dense canopy. (b) Photosynthetic action spectrum for a higher plant. Adapted with permission from ref 64, p 183. Copyright 2005 Pearson Education, Inc. (c) Absorption spectra of photosynthetic pigments utilized in light harvesting.65,66 (d) Chemical structures of the chlorophyll, carotenoid, and phycobilin pigments. Adapted with permission from ref 37. Copyright 2015 Springer. photosynthesis.13,14 For example, purple sulfur bacteria utilize dependent” and “light-independent” reactions is hazy, to say hydrogen sulfide or thiosulfate as the electron donor, whereas the least. purple nonsulfur bacteria consume organic compounds, such as Robert Emerson and William Arnold performed pioneering fatty and amino acids.15 In fact, many studies have concluded experiments, in 1932, exposing a suspension of the green alga that oxygenic photosynthesis appeared later, having evolved Chlorella pyrenoidosa to a series of light flashes and measuring from anoxygenic photosynthesis, because geochemical evidence the maximum oxygen evolution.19 Their surprising findings points strongly to a largely anoxic atmosphere up until the suggested that about 2500 chlorophyll (Chl) molecules are “Great Oxidation Event”, which occurred about 2.4 billion years involved in the production of a single molecule of oxygen. In ago.16 1934, Arnold and Henry Kohn, after examining several other The three stages of photosynthesis take place in the presence photosynthetic systems, confirmed the existence of a “unit” of of light: (1) light harvesting from sunlight; (2) use of that ∼2400 Chl molecules per oxygen molecule, calling it a energy for the production of ATP and reducing power, reduced “chlorophyll unit”.20 In 1936, Kohn concluded that the physical ferredoxin, and NADPH; and (3) capture and conversion of number of chlorophylls in a chlorophyll unit was closer to 500, CO2 into carbohydrates and other cell constituents. However, a number consistent with the idea developed by Warburg and the only true light reactions are over when charge separation Negelein (1922) that four photons were required for the has ended at the reaction centers (see, e.g., Govindjee and production of oxygen.21,22 The controversy over the minimum Govindjee, 1974).17 During the third stage, namely, the carbon quantum requirement for oxygen evolution and the opposing reactions, long incorrectly designated as the “dark reactions” or views of Warburg and Emerson were reviewed in a nice “light-independent reactions”, the energy-rich products of the historical perspective by Nickelsen and Govindjee (2011)23 and ̈ 24 light reactions are used to reduce CO2. Certain enzymes of the summarized by Karin Hill and Govindjee (2014). Also in carbon reactions require light for regulation (see, e.g., Wolosiuk 1936, Hans Gaffron and Kurt Wohl expanded on Emerson and and Buchanan, 2015).18 Thus, the division of even “light- Arnold’s 1932 experiment, where exposure of a Chlorella C DOI: 10.1021/acs.chemrev.6b00002
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