structure and energy transfer in photosystems of oxygenic … · 2015-06-26 ·...

BI84CH24-Nelson-Junge ARI 24 April 2015 10:51

Structure and Energy Transferin Photosystems of OxygenicPhotosynthesisNathan Nelson1 and Wolfgang Junge2

1Department of Biochemistry, George S. Wise Faculty of Life Sciences, Tel Aviv University,Tel Aviv 69978, Israel; email: [email protected] of Biophysics, Universitat Osnabruck, DE-49069 Osnabruck, Germany

Annu. Rev. Biochem. 2015. 84:659–83

First published online as a Review in Advance onMarch 5, 2015

The Annual Review of Biochemistry is online atbiochem.annualreviews.org

This article’s doi:10.1146/annurev-biochem-092914-041942

Copyright c© 2015 by Annual Reviews.All rights reserved

Keywords

photosynthesis, light harvesting, electron transfer, membrane complexes,structure, chloroplasts, cyanobacteria

Abstract

Oxygenic photosynthesis is the principal converter of sunlight into chem-ical energy on Earth. Cyanobacteria and plants provide the oxygen, food,fuel, fibers, and platform chemicals for life on Earth. The conversion ofsolar energy into chemical energy is catalyzed by two multisubunit mem-brane protein complexes, photosystem I (PSI) and photosystem II (PSII).Light is absorbed by the pigment cofactors, and excitation energy is trans-ferred among the antennae pigments and converted into chemical energyat very high efficiency. Oxygenic photosynthesis has existed for more thanthree billion years, during which its molecular machinery was perfected tominimize wasteful reactions. Light excitation transfer and singlet trappingwon over fluorescence, radiation-less decay, and triplet formation. Photo-synthetic reaction centers operate in organisms ranging from bacteria tohigher plants. They are all evolutionarily linked. The crystal structure de-termination of photosynthetic protein complexes sheds light on the variouspartial reactions and explains how they are protected against wasteful path-ways and why their function is robust. This review discusses the efficiencyof photosynthetic solar energy conversion.

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Contents

INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 660ADVANCES IN STRUCTURAL BIOLOGY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 661PHOTOSYSTEMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 662

A Scenario for the Evolution of Photosynthetic Reaction Centers . . . . . . . . . . . . . . . . . 662Structure and Function of Photosystem I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 666Functional Organization of Light-Harvesting Complex I . . . . . . . . . . . . . . . . . . . . . . . . . 667Light Absorption and Excitation Transfer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 669Excitation Transfer Among the Light-Harvesting Proteins of Purple Bacteria . . . . . 669Excitation Transfer in Light-Harvesting Complex II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 670Excitation Transfer in Reaction Centers of Oxygenic Photosynthesis . . . . . . . . . . . . . . 671Excitation Transfer in Photosystem II Complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 672Excitation Transfer in Cyanobacterial Photosystem I Complexes . . . . . . . . . . . . . . . . . . 673Excitation Transfer in Eukaryotic Photosystem I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 674

INTRODUCTION

Oxygenic photosynthesis in cyanobacteria, algae, and plants is accomplished by a series of reac-tions catalyzed by large membrane protein complexes, soluble factors, and electron donors andacceptors. The reaction velocities of the primary processes span a wide time range. The wholereaction cascade—which covers light absorption by pigment cofactors, excitation energy transferamong antennae, electron transfer (ET) within and between photosystems, proton transfer, ATPsynthesis, carbon fixation, and the export of stable products—ranges from femtoseconds (10−15) topicoseconds (10−12), nanoseconds (10−9), microseconds (10−6), milliseconds (10−3), and seconds.The photochemical reactions operate in the range of femto- to nanoseconds, and the biochemicalreactions operate on the microsecond-to-second scale. One of the most important properties ofoxygenic photosynthesis is its ability to orchestrate all of those processes while minimizing lossand damage.

Photosynthesis spans the widest range of redox potential in the biochemistry of life, as it canproduce the most oxidative reaction [water oxidation by photosystem II (PSII); ε0′ = +0.8, whereε0′ is the standard redox potential at 25◦C] and the most powerful reducing compound [ferredox-ins by photosystem I (PSI); ε0′ = −0.4]. Operation under extreme redox potential presents anenormous challenge, mainly for protection against damage by highly reactive components such assinglet oxygen, which is a by-product of the photochemical activity, as well as loss of high-energyelectrons to nonproductive components in the environment.

All of these challenges have been addressed in various ways by the long evolution of oxygenicphotosynthesis, which is reflected in the fine structure of its components. Determination of theatomic structure of the photosynthetic complexes in several organisms that thrive in differentenvironments shows how each component copes with the specific challenges it faces.

The mechanism of each reaction depends on its specific respective time domain. The photo-physical and photochemical reactions that occur between femtoseconds and nanoseconds are gov-erned by quantum mechanics. Those that occur between microseconds and seconds are governedby electrostatics and statistical mechanics. Despite nature’s general tendency to avoid wastefulreactions, some leaks and slips are used to control the production rates; quite often they becomea necessity and a vehicle for advancing the evolution of elaborate systems (1).

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This review attempts to capture the excitement generated by the determination of the three-dimensional structures of the photosystems that catalyze oxygenic photosynthesis. Several recentreviews contain detailed discussions and list original references to earlier research (2–12). We focuson the photosystems of higher plants, but we also refer to the wealth of structural informationthat is available on the photosystems of thermophilic cyanobacteria, especially in the case of PSII,for which a plant crystal structure has not yet been obtained.

Regarding the function of the photosystems, we focus on excitation energy transfer andtrapping; the mechanisms of ET have been described elsewhere. Briefly, ET between fixedcofactors within the photosystems occurs by a nuclear electron tunneling mechanism, as describedby Marcus (13) and Marcus & Sutin (14). Over more than 12 orders of magnitude, the rateis exponentially related to the edge-to-edge distance between the cofactors in the respectiveproteins (15, 16). Detailed structural information is necessary to understand the mechanism ofaction of photosynthetic systems.

ADVANCES IN STRUCTURAL BIOLOGY

Before discussing the photosystems of plants, we begin with a short survey of recent advancesof structural biology. Recent developments in electron tomography and single-particle analy-sis enabled advances in this important research direction. Electron tomography is an extension oftransmission electron microscopy, in which a beam of electrons is passed through a sample at incre-mental degrees of rotation; the information is collected and used to assemble a three-dimensionalimage of the target. This technique has been successfully adapted to biological materials, butits resolution initially ranged between 50 and 200 A (17). Improvements in electron microscopy(EM) and especially in the detection system advanced the method up to atomic resolution insolid material and close to atomic resolution in biological DNA and protein complexes (18, 19).In these studies, three-dimensional particles identified in biological organelles were fitted withknown three-dimensional structures, usually obtained by X-ray crystallography; this process re-vealed the distribution and organization of the protein complexes. The approach revolutionizedour perspective of several aspects of membrane architecture and provided previously unobtainableinformation. A prime example is the organization of ATP synthase in chloroplast and mitochon-drial membrane and its influence on the structure of thylakoids and cristae in their respectiveorganelles (20).

Structure determination by electron diffraction of membrane proteins using two-dimensionalcrystals is a highly promising technique (21, 22). Whereas X-rays travel through a thin two-dimensional crystal without diffracting significantly, electrons can be used to form an image (23).Conversely, the strong interaction between electrons and proteins renders this technique uselessfor thick (1-μm) crystals. Therefore, proteins such as bacteriorhodopsin, which forms orderedtwo-dimensional arrays in vivo, became the first subjects of high-resolution EM structures. Thistechnique was used to determine the structure of light-harvesting complex II (LHCII) (24). Theeventual crystal structures of LHCII and its homolog CP29 by X-ray crystallography yieldedsuperior structural information (25–27). Not only did the resolution increase from 3.4 to 2.5 A,but also the quality of the model significantly improved.

Recent advances in single-particle cryo-EM and electron tomography promise to provide un-precedented structural information about intact membrane complexes (28–30). Electron tomogra-phy studies have revealed the rowlike organization of ATP synthase in mitochondrial membranes(31, 32), supporting the idea (33) that the interaction between these complexes determines thecurvature of the membranes (19, 34, 35). Future electron tomography studies are likely to yieldvaluable information about the fine structure and dynamic of photosynthetic membranes.

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Improvements in cryo-EM and data processing will revolutionize structural biology. Cryo-EMwas used to determine the structure of the large subunit of mitochondrial ribosome at near-atomicresolution, demonstrating that this technique can provide information of comparable quality toX-ray crystallography but requires much smaller amounts of more heterogeneous material (36,37). Cryo-EM is likely to dominate structure determination of large (∼1-MDa) complexes andto gradually replace X-ray crystallography in such studies. However, we must be cautious not tooverinterpret these results. The main advantage of X-ray crystallography is that, quite often, allthe purified protein in the well ends up in the crystal (38). Consequently, one can solubilize thecrystals and verify that the structural information was obtained from an active protein. Moreover,photochemical activity can be analyzed in the crystals of photosynthetic complexes (39). Thisactivity-verification approach is not possible with cryo-EM. The small proportion of the singleparticles selected for improved resolution poses a greater challenge. In this case, one could solvethe structure of a conformation or substate that is irrelevant to the in vivo active complex. Thisdrawback also applies to electron tomography.

Improved detection and analysis of electron diffraction may become an important tool for futurestructure determination at atomic resolution. In a study that subjected small lysozyme crystals tocryo-EM electron diffraction, electron diffraction data were collected at 1.7-A resolution, and thestructure was refined to 2.9-A resolution (40). During crystallization of membrane proteins, oneoften obtains relatively large but thin (∼1-μm) crystals that are useless for X-ray crystallographybut potentially amenable to electron diffraction and cryo-EM structure determination. Thus,combinations of all these techniques, including X-ray and electron diffraction, cryo-EM, andelectron tomography, are necessary for a deep understanding of structural biology.

PHOTOSYSTEMS

A Scenario for the Evolution of Photosynthetic Reaction Centers

Biological systems involved in electron transport operate in redox potential boundaries. Oxygenicphotosynthesis operates at the most extreme redox potentials of +1.0 to −1.0 V, but the reactionsin these extremes last for <1 ns. The proteins that operate at extreme redox potentials are likely tobe damaged or to inflict damage by oxidation, radical formation, or breaking of chemical bonds.So far, very little is known about the structure determinants that prevent the oxidation of solubleamines at +1-V redox potential or, more importantly, the “stealing” of electrons by oxygen at−1-V redox potential. Over time, evolution has coped with these challenges, and membranecomplexes largely mitigate potential damages. Thus, the evolution of each complex aimed notonly to maximize efficiency but also to minimize potential damage (41).

The two main complexes that produce or use oxygen, PSII and cytochrome oxidase, meet theabove challenges by an entirely different mechanism. Similarly, PSI, which produces NADPH,and the respiratory complex I, which utilizes NADH, are not alike in any respect. In contrast, thecytochrome bc complex, which operates at mild redox potentials, has homologs in most photosyn-thetic and respiratory electron transport chains, and it may serve as an evolutionary template forall those systems. We argue that the main active units representing the major bioenergetics com-plexes began to evolve in the prebiotic world and, consequently, that current DNA and proteinsequences do not bear on their early evolution (42). Rather, the basic chemistry of redox reactionsand mechanical machineries, reflected in the fine structure of the current complexes, initiatedthe evolution of the various partial reactions that eventually assembled into the wide variety oftoday’s bioenergetics processes. Because the cytochrome bc complex operates at neutral redoxpotentials, it probably provides the template for a primordial electron transport chain. However,

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under anaerobic conditions, in which almost every chemical is reduced, electron acceptors arescarce (43). Therefore, positive potential provided by emerging photosynthetic reaction centers(RCs) was a necessary step in the evolution of bioenergetic systems.

The Sun provides more than 100,000 TW of light power to the surface of the Earth. Ev-ery pigment is subject to photochemical processes, including “productive” processes such as thegeneration of new components and energy for biological (including human) activities. Photosyn-thesis evolved to maximize these productive processes. Today, photosynthesis provides more than150 TW (on land and in the oceans) of chemical energy. That is 10 times more than humans’global consumption of primary energy. In most current photosynthetic processes, light energy isconverted into chemical energy by photosynthetic RCs (3, 44, 45). RCs operate in organisms rang-ing from bacteria to higher plants. They are all evolutionarily linked, as demonstrated by partialamino acid sequence homologies and especially by their fine structure (42, 46). The core of everyphotochemical RC is a dimeric structure, and RCs’ evolution probably began with a homodimericstructure and progressed from symmetry through pseudosymmetry to asymmetric structures (47).The diversity of the present-day RCs poses a challenge to the determination of their origin, butthe greater availability of genomic sequences and of high-resolution crystal structures of RCs fromvarious organisms enable us to imagine a scenario for their common evolutionary path.

Currently, there are two main types of RCs that can be differentiated by their electron acceptors.In type I, excited electrons are captured by electron acceptors such as ferredoxin. In type II,excited electrons are captured by loosely bound quinone. Type I includes the PSIs of oxygenicphotosynthesis and some bacterial phyla, such as Chlorobi. Type II includes the PSIIs of oxygenicphotosynthesis and bacteria, such as purple bacteria. Figure 1 depicts some available structures of

a b

c d

Figure 1Available structures of RCs from various sources, adjusted to the relative size of plant PSI. These structuresrepresent monomeric forms containing a single charge-separation electron transport chain. (a) SynechocystisPSI (PDB 4L6V). (b) Pea plant PSI (PDB 3LW5). (c) Rhodopseudomonas palustris RC–LH1 complex (PDB1PYH). (d ) Synechococcus vulcanus PSII (PDB 3ARC). Abbreviations: LH1, light-harvesting 1 complex; PDB,Protein Data Bank; PSI, photosystem I; PSII, photosystem II; RC, reaction center.


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PscA PsaB PsaA

CP43

D2

D1

CP47 L

M

PscA

PSI RC PSII RC Bacterial RCHomodimeric RC

Primordial heterodimeric RC

Primordial homodimeric RC

1

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Figure 2A proposed scenario for the initial evolution of photosynthetic RCs. � A homodimeric PSI composed of two PsaA-like subunits withone FeS cluster as an electron acceptor. This type of homodimeric RC currently functions in Chlorobi, heliobacteria, andacidobacteria. � Gene duplication resulted in two nonidentical PsaA and PsaB subunits (coordinates from PDB 1JB0). � A similarcore is present in the heterodimeric PSI of cyanobacteria, algae, and plants. � PsaB split into D1 and CP43, and PsaA split into D2and CP47 to form the core complex of PSII. The FeS cluster was substituted by an iron atom (coordinates from PDB 3ARC).� Following the split in step �, CP43 and CP47 were lost and substituted by different light-harvesting systems to form the core of thebacterial RCs (coordinates from PDB 4RCR). Abbreviations: PDB, Protein Data Bank; PSI, photosystem I; PSII, photosystem II; RC,reaction center.

RCs from various sources. Clearly, they evolved far apart from one another. However, sequenceinformation about proteins involved in photochemical activity revealed a link between both type II(48) and type I RCs (49–51). The center of PSI is composed of two homologous chlorophyll–protein subunits. Four out of its 11 transmembrane helices are homologous to those in the centerof PSII as well as to the bacterial RC, and another five may be related to the primary antennasubunits of PSII (47, 52). All of these initial observations and assumptions were confirmed by thehigh-resolution structures of the various RCs (38, 53–58). The discovery that Chlorobium RC ishomodimeric gave credence to the notion of a common ancestor for all photosynthetic RCs (49).

Figure 2 depicts a scenario for the common evolution of all photosynthetic RCs. Clearly, allthe heterodimeric RCs are likely to have evolved from a homodimeric one. The primordial RCmay have been a homodimeric unit resembling the core complex of the current RCs in Chlorobi,heliobacteria, and acidobacteria (42, 49, 59–61). Thus, homodimeric RCs probably preceded themore complex heterodimers of the type I and type II RCs. Gene duplication, followed by theevolution of a heterodimeric structure, probably led to the advanced RCs found in cyanobacteria

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and plants (49). Gene duplication and subsequent separate evolution of the two genes are commonin higher-order systems, which are subjected to ever-increasing regulatory processes that arebetter able to react to environmental changes (47). Following this argument, the primordial PSI-like homodimeric RC was the origin of all RCs, including those of PSI and PSII as well as thatof bacteria, and it functioned primarily in cyclic photophosphorylation (49, 60). The primordialPsaA and PsaB subunits diverged to the current PSI core complex of cyanobacteria, algae, andplants. Concomitantly, PsaB split into D1 and CP43, and PsaA split into D2 and CP47 to formthe core complex of PSII. An iron atom situated between two quinones, of which one is tightlybound and the other loosely bound, substituted for the iron–sulfur cluster. A few mutations inD1 formed the site of the manganese cluster, and oxygenic photosynthesis was initiated. In thebacterial RC, CP43 and CP47 were lost and substituted by different light-harvesting systems (62).The core of the bacterial RC, with its L and M subunits, maintained the sequence and structuralrelationships to D1 and D2 of PSII.

The long evolution of the various RCs generated more subunits (Figure 3), and currentcomplexes contain up to 20 different subunits. Each evolved to maximize light absorption and

PsaGPsaK

PsaA

PsaH

PsaB

Lhca1

Lhca4 Lhca2

Lhca3

Figure 3A view of the structure of plant photosystem I from the stromal side. The structural coordinates are fromProtein Data Bank entry 4RKU. The chlorophyll molecules of the core complex are shown in cyan,light-harvesting complex I in magenta, the gap chlorophylls in brown, lipids in purple, and the carotenoidsin blue. The protein backbone of the 17 subunits and the positions of PsaA, PsaB, PsaG, PsaH, PsaK, andLhca1–4 subunits are also shown.


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energy conversion under greatly variable light intensities and temperatures and often-hostileenvironments.

Structure and Function of Photosystem I

PSI is defined as the membrane chlorophyll–protein complex that catalyzes the light-dependentreaction of plastocyanin (or c-type cytochrome) oxidation and ferredoxin reduction. Current or-ganisms contain this functional complex in different but evolutionarily related forms. The mostbasic structure in all those complexes is a symmetric or pseudosymmetric assembly of one or twochlorophyll-containing proteins, which are covalently bound through iron–sulfur clusters thatserve as electron acceptors (49, 63). Remarkably, one of the simplest reactions in nature—thatphotoabsorption followed by generation of excited electron—is executed in plant PSI by a 650-kDa complex containing up to 18 subunits and more than 200 prosthetic groups (38). The electrondonors of PSI, plastocyanin and cytochrome c553, bind to PSI through a hydrophobic interactionwith PsaA and PsaB and through an electrostatic interaction with the N terminus of PsaF (seeReferences 7 and 64 and references therein). In cyanobacteria, the contribution of the latter isminor and is specific for plastocyanin. Under normal conditions, the rate of P700 reduction bycytochrome c553 is identical in wild type and a mutant lacking the PsaF N terminus (58, 65, 66).The building of PSI involves a very complicated biogenesis and assembly process that brings allthe PSI components together to generate the most efficient photochemical machine in nature(67–69).

The most recent X-ray crystal structure [at 3.1-A resolution; ambiguous PsaR and chlorophyllmolecules were deleted (PDB 4RKU)] of the monomeric plant PSI complex revealed 17 proteinsubunits containing 45 transmembrane helices, which comprised 158 chlorophylls, 28 carotenoids,2 phyloquinones, 8 lipid molecules, and 3 Fe4S4 clusters (Figures 3 and 4). Remarkably, PSIhas an extremely high nonprotein content. Approximately one-third of the total mass of thecomplex consists of different cofactors, such as chlorophylls, carotenoids, phyloquinones, andFe4S4 clusters. Several genetic, biochemical, and spectroscopic studies have shown that numerouscofactors are important not only for the function of PSI but also for its structural integrity (70, 71).The RC and light-harvesting complex I (LHCI) form two distinct and loosely associated moieties,with a deep cleft between them. Functions of different subunits of the RC have been described (48,72, 73). The two major proteins in the complex are the large subunits PsaA and PsaB. They forma heterodimer consisting of 22 transmembrane helices, which harbor most of the cofactors of theelectron transport chain (from the special chlorophyll pair denoted P700 to the first Fe4S4 cluster,Fx), forming the heart of the complex. In addition, the heterodimer coordinates more than 80chlorophylls that function as the intrinsic light-harvesting antennae. The stromal subunit PsaCcarries the two terminal iron–sulfur clusters, and together with PsaD and PsaE it participates inthe docking of the stromal electron acceptor, ferredoxin (74–76). PsaF contributes to the bindingof the luminal electron donor, plastocyanin, and may participate in excitation energy transfer fromLHCI to the core complex (77). PsaG is an anchor for LHCI binding. PsaJ is important for thestability and assembly of the PSI complex (78). PsaH, PsaI, and PsaL constitute the domain ofinteraction with LHCII during the state transitions. In addition, PsaH prevents trimer formation(see Reference 71 and references therein).

LHCI is composed of four nuclear gene products (Lhca1–4), which are assembled into twodimers in a half-moon-shaped belt that docks to the core PsaF side. The LHCI belt contributes amass of 180 kDa (out of ∼650 kDa). Lhca1–4 polypeptides belong to the LHC family of chlorophyllab–binding proteins (see References 7 and 64 and references therein). The binding between theLhca proteins does not involve any helix–helix interactions but creates a head-to-tail arrangement

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PsaH

PsaA

PsaK

PsaG

PsaB

Lhca3

Lhca2Lhca4

Lhca1

Figure 4A view from the stromal side of the prosthetic groups of plant photosystem I. The annotations are the sameas those in Figure 3. The protein chains have been removed; the unambiguous prosthetic groups identifiedto date are shown.

that maximizes the number of chlorophylls facing the RC (79). PsaN is located on the luminalside of the complex. Its role is not well understood, although it may be involved in the docking ofplastocyanin (80, 81). Its location suggests a possible interaction with LHCI, but it does not seemto be involved in the assembly of additional light-harvesting proteins, such as Lhca5 (79).

Functional Organization of Light-Harvesting Complex I

One of the most important aspects of plant PSI structure is the arrangement of the four light-harvesting proteins (82–84). The four proteins of LHCI ligate chlorophylls and carotenes, whichabsorb light and transmit the excitation energy to the core complex. The sequence of the fourLHCI subunits is Lhca1, Lhca4, Lhca2, and Lhca3 (82, 83); Lhca1 interacts with PsaG andLhca3 with PsaK (Figure 5). Nelson and colleagues (47) have proposed that PsaG served as atemplate for the assembly of Lhca monomers during the early evolution of LHCI. In the currentRC, the assembly of LHCI is apparently less PsaG dependent. An intriguing question is whynature provided PSI with four different gene products to perform the same role. To answer thisquestion, we have to examine the interface between the RC and the LHCI belt and consider anoptimal excitation transfer from the Lhca subunits and the RC. The asymmetrical arrangementof this interface, formed by PsaG, PsaA, PsaF, PsaJ, PsaB, and PsaK (Figure 5), was dictatedby evolutionary steps that shaped advanced photosynthetic life forms from primitive organisms(47, 83). Consequently, different types of interactions evolved at each section of the interface for


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LH2

RC–LH1

Figure 5Distribution of LH2 (PDB 2FKW) and the RC–LH1 complex (PDB 1PYH) in the membranes ofphotosynthetic bacteria. Abbreviations: LH1, light-harvesting 1 complex; LH2, light harvesting 2 complex;RC, reaction center.

optimal binding and probably refurbishing of damaged Lhca subunits. Lhca1 attaches to the corethrough PsaB, and the helix–helix bundle forms with the transmembrane helix of PsaG. Lhca4’sinteraction with the RC is mediated mainly through gap chlorophylls coordinated by the V-shapeddomain of PsaF. Lhca2 protrudes its stroma-exposed N termini into the PsaA subunit and interactsthrough the gap chlorophyll, coordinated by PsaJ. Lhca3 has some structural peculiarities, whichmay be why it provides the purest electron densities obtained for PSI subunits. Lhca3 interactswith PsaK (see References 7 and 64 and references therein), a finding supported by our model.Because this part of the supercomplex is less resolved, we cannot identify the precise contacts ofLhca3, and it is likely that this site is occupied partly by yet another gene product, such as Lhca5(85). Lhca1–4 share considerable amino acid sequence homology, as well as structural similarity,with LHCII proteins (25, 26, 38, 86). Despite this background, these proteins display differentoligomerization behaviors and have several unique properties.

Numerous biochemical experiments, spectroscopic studies, molecular dynamics simulations,and homology modeling approaches have attempted to reveal the character of Lhca1–Lhca4 andLhca2–Lhca3 heterodimerization (see References 7 and 64 and references therein). Unfortunately,the best resolution of the PSI crystal structure is not sufficient to obtain near-atomic resolutionof this part of the plant PSI supercomplex. Only a higher-resolution structure revealing the en-tire chlorophyll transition dipole moments; complete phytol chains; and the positions of luteins,

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violaxanthins, and lipid and water molecules will provide a comprehensive characterization ofthese interactions.

Light Absorption and Excitation Transfer

All photosynthetic processes involve the generation of excitations by absorption of photons andthe transfer of this excitation to the RC, where ET takes place. This transfer of energy from theabsorption site to the reaction site is known as light harvesting and is highly efficient; at low lightintensity, more than 99% of the absorbed photons lead to charge separation at the RC. Whereasphoton absorbance and the generation of the initial excited state last for a few femtoseconds,the stable charge separation occurs at the nanosecond scale. For more than 50 years, the pho-tosynthetic excitation transfer was explained by incoherent classical hopping (Forster transfer)from one chromophore to the next (87). Because the pigments in antennae complexes are closetogether, wave-function overlap delocalizes the excitation over several pigments (coherent excita-tion transfer). Intra- and intermolecular vibrations of pigments and protein vibrations (dynamicdisorder) rapidly delimit the coherence in the antennae within ∼10 fs, causing the excitation andtransfer to localize by a series of independent hops at longer timescales (see Reference 88 andreferences therein). Surprisingly, once the excitation reaches the very core of the RC, longer-lasting coherence may become important. In a recent study of the core of PSII (with only fourchlorophylls and two pheophytins present), long-lasting (picosecond-duration) quantum beatswere observed. The coherence between vibronic and charge transfer states may be pivotal for mul-tichannel passage into the metastable charge-separated state at nearly 100% quantum efficiency(89).

Excitation Transfer Among the Light-Harvesting Proteins of Purple Bacteria

The primary reactions of purple bacterial photosynthesis take place within two well-characterizedpigment–protein complexes: the core RC–LH1 (light-harvesting 1 complex) and the more pe-ripheral LH2 (light-harvesting 2 complex). Typically, light energy is absorbed by LH2 and is thentransferred via LH1 to the RC. The antenna complexes are generally composed of two types ofpolypeptides (α and β chains), which are arranged in a ringlike fashion, creating a membrane-embedded cylinder. All species of purple bacteria contain a “core” antenna complex, LH1, thatsurrounds the RCs. Most species also contain a second type of antenna complex, LH2, which isarranged more peripherally (Figure 5). The exact ratio of LH2 to LH1 in the photosyntheticmembrane is controlled by various environmental factors, such as light intensity (90, 91). LH2typically has two strong absorption bands in the near-IR region, at 800 and at 820 or 850 nm. A rel-atively low-resolution crystal structure of the RC–LH1 core complex (56, 92) and high-resolutioncrystal structures of LH1 and LH2 are available (93). These data, together with the circular sym-metry of LH2, have prompted numerous theoretical and experimental studies of excitation transferwithin and out of LH2.

Studies on the excitation of the B850 ring (the spectral form at 850 nm) demonstrated that de-localized excitations persist across several pigment molecules (see Reference 94 and referencestherein). These studies showed quantum coherence within each of the two rings and raisedthe possibility of coherent coupling between the rings. The use of polarization-controlled two-dimensional spectroscopy, which allows observation of only the coherent electronic motions,revealed a persistent coherence among all states and assigned ensemble dephasing rates for thevarious coherences (95). Although such measurements may influence the results of quantum-mechanical experiments, the data strongly support the involvement of coherent excitation transfer


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Figure 6Excitation transfer from light-harvesting 2 complex to the reaction center of photosynthetic bacteria.

within LH2 (96). The biological relevance of those theoretical and experimental approaches isstill uncertain, but intuitively they make sense.

It is primarily the intercomplex, and not the intracomplex exciton transfer, that is criticalfor overall efficiency. Here, too, a coherent excitation transfer among the many LH2s, as wellas the excitation transfer to the RC–LH1 complex, seems logical but is experimentally muchmore challenging to demonstrate. From a biological perspective, such a mechanism may involvecoherent delocalization of the excited state in pairs of chlorophyll molecules (Figure 6). Theexcited state hops internally in LH2 and among the neighboring complexes until it reaches LH1,where the excited electron is captured inside the RC to generate a stable charge separation. Ifsuch a mechanism exists, it would depend strongly on the environment within and outside thecomplexes to generate a constrictive phonon. Evolution over a long period of time could generatethe required phonon composition for effective excitation transfer.

Excitation Transfer in Light-Harvesting Complex II

LHCII, one of the most abundant proteins on Earth, essentially gives our planet color (97). Someof the LHCII is bound as an excitation transfer complex with PSII, but a significant portion moves

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in the membrane or is temporarily bound to PSI (98–101). In photosynthetic membranes, LHCIImay be present in a monomeric form that contains ∼12 chlorophyll molecules and a trimeric com-plex form. These free complexes may lose light-absorbed energy to heat or nonphotochemicalquenching (102–106). Several site-directed mutagenesis studies of chlorophyll-binding residues inreconstituted LHCII indicated that five binding sites occupy chlorophyll a, three occupy chloro-phyll b, and an additional four can bind both (107–110). In contrast to the symmetric arrangementin the bacterial LH2, the highly inhomogeneous spectra and the multicomponent energy transferkinetics in LHCII present a very complicated and puzzling problem. The asymmetric pigment lo-calization and orientation in LHCII resemble those of aggregates (26). For molecular aggregates,electronic coherence effectively delocalizes excitations over one or several chromophores, whereasdephasing leads to localization of the energy. The dense packing of pigments produces electrody-namic couplings between pigments. These couplings are highly sensitive to both molecular struc-ture, which determines the pathways, and the mechanisms by which energy is transferred from aninitial absorption to the target molecule, as exemplified by multichromophoric light-harvestingproteins such as LHCII and its homologs. Elaborate spectroscopic studies led to a proposal of anexciton model for LHCII that enables determination of the timescales and pathways of energytransfer (111). In this model, individual exciton states can be delocalized over 2 to 2.5 molecules inthe chlorophyll a region, and thermal mixing results in a coherence size of 1.4 to 1.8 molecules forthe steady-state wave packet at room temperature. Evidence from two-dimensional femtosecondspectroscopy performed on solubilized LHCII suggests that this protein transfers photoexcitationwith high efficiency through interplay between excitonic quantum coherence, resonant protein vi-brations, and thermal decoherence, even at physiological temperatures (112–115). Similar resultswere obtained with the CP29 LHC, which is a homolog of LHCII but function as a monomer inthe PSII complex (116). Structural parameters indicate coherence lengths up to 5 nm, consistentwith the sizes of LHCII and part of the RC. However, a semiconductor quantum dot–like networkengineered with hierarchically clustered structures and small static disorders may support coher-ent excitation transfer over greater length scales at ambient temperatures. The thylakoid granastacking may represent such an assembly, which facilitates excitation transfer not only amongpigment–protein complexes within a given membrane but also between PSII complexes situatedin the grana in adjacent membranes.

Excitation Transfer in Reaction Centers of Oxygenic Photosynthesis

As mentioned above, densely packed pigment–protein complexes absorb and then translocatephotoenergy via electrodynamic couplings between pigments toward a central site of charge sep-aration, known as the RC (117). Most ultrafast and two-dimensional femtosecond spectroscopystudies have been performed with FMO (47, 118, 119) and LHCII, which contain 7 and 12 chloro-phyll molecules, respectively. Thus, it is very challenging to apply the techniques developed forthe study of relatively simple complexes to the study of PSI and PSII of oxygenic photosynthesis.Structural information, in particular information about the geometry of the chlorophyll array,enabled the construction of microscopic models for the excitation transfer network (117, 120–123). Once the location and orientation of pigments are determined, excitation transfer ratesbetween pigments can be described well by Forster theory (87). Redfield theory or modified Red-field equations (111, 124) provide an alternative description that is relevant for strong couplingsand fast timescales. Modified Redfield equations could minimize the perturbation term associatedwith electron–phonon coupling. Considering coherent excitation transfer potentially may solvesome problems derived from the rigid reliance on population kinetics predicted by the aboveformulations (125).


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–

+

Figure 7Excitation transfer and charge separation in photosystem II (PSII). The coordinates were taken from Synechococcus vulcanus PSII(Protein Data Bank identifier 3ARC). Chlorophylls are in cyan, pheophytins in magenta, and quinones in yellow. Iron molecules arerepresented as red spheres, and manganese clusters are shown as purple and red spheres. Tyrosine D161 also is shown. The delocalizedelectron is depicted as a yellow/red cloud. The chlorophyll on the right is the closest to the primary light-harvesting part of PSII.

The PSII RC, composed of D1, D2, and cytochrome b559, is structurally related to the pur-ple bacteria RC (48, 127). Also, the high-resolution structure of cyanobacterial PSII providedthe presumed exact position and orientation of the chlorophylls of the plant RC. Several re-cent experiments of two-dimensional light and electronic spectroscopy took advantage of thisfact and revealed coherent excitation phenomena in the plant PSII RC. Myers et al. (128) usedtwo-dimensional electron spectroscopy (2DES) to study the D1–D2–cytochrome b559 PSII RCcomplex. They observed rapid (50–150-fs) energy equilibration throughout the PSII RC and aheterogeneous distribution of 1 to 3 ps associated with charge transfer. Moreover, they reportedenergy transfer of 6 to 8 ps from states absorbing nearly 670 nm, consistent with transient absorp-tion studies that attributed a 14-ps process to slow energy transfer from one or more pigmentsto other pigments, including P680, followed by rapid charge separation (129). Using a similarpreparation of the PSII RC, analyzed by transient absorption experiments at 77 K with variousexcitation conditions, investigators observed at least two different excited states giving rise to twodifferent pathways for ultrafast charge separation (130). The authors proposed that the disorderproduced by slow protein motions causes energetic differentiation among RC complexes, leadingto different charge-separation pathways.

Surprisingly, once the excitation reaches the very core of the RC, longer-lasting coherencemay become important. A recent study of the core of PSII (with only four chlorophylls andtwo pheophytins present) observed long-lasting (picosecond-duration) quantum beats (89). Thecoherence between vibronic and charge transfer states may be pivotal for multichannel passageinto the metastable charge-separated state at nearly 100% quantum efficiency (89). Figure 7illustrates probable steps in excitation transfer and charge separation in the PSII RC. This studyrelates to the very core of PSII. The excitation transfer between LHCs and from LHC to this RCis slower and probably does not involve coherence.

Excitation Transfer in Photosystem II Complexes

Excitation transfer within the various PSII complexes is much more complex than in the PSIIRC. In most of the publications on this subject, the preparation used for the experiments is notdefined. In order to evaluate the results, it is critical to know the integrity of the photosystemsused for the experiments, even if they were conducted at 77 K. Ideally, reliable conclusions wouldbe drawn on the basis of a crystal structure; therefore, such experiments should be performedon diffracting crystals (39). These experiments could be carried out with cyanobacterial PSII, forwhich high-resolution crystals are available (54, 55, 131).

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Cyanobacterial PSII is composed of 17 transmembrane subunits, 3 peripheral proteins, andseveral cofactors; its total molecular weight is 350 kDa. The light-induced oxidation of water iscatalyzed by a Mn4Ca cluster that cycles through several different redox states (S0 to S4) followingextraction of each electron by the PSII RC P680 chlorophyll assembly. The dimeric structure ofcyanobacterial PSII revealed 20 protein subunits, 35 chlorophyll a molecules, and 12 carotenoidmolecules per monomer. Most of the chlorophyll molecules are bound to the intrinsic antennaproteins CP43 and CP47. The assembly of 70 chlorophylls, arranged in pseudo-twofold symmetry,presents an enormous challenge for 2DES studies; plant PSII is much more complicated thancyanobacterial PSII (48, 132). In addition to the chlorophyll-containing subunits in cyanobacterialPSII, the plant PSII monomer contains at least one LHCII trimer, one CP26 monomer, andone CP29 monomer. PSII contains ∼95 chlorophylls and 30 carotenoids per RC. Although apure and active preparation of plant PSII (known as BBY particles) is available (48, 133), it is notmonodisperse and is difficult to freeze-store without a significant loss of activity. Several excitationtransfer experiments have been performed with BBY particles, and even intact membranes, but2DES experiments cannot be carried out in such complicated and unstable systems.

Excitation energy transfer studies with plant and alga PSII have used genetics and molecularbiology tools to unravel the complexity of the system. One such study searched for the effect ofantenna depletion on excitation transfer in Arabidopsis thaliana mutants (134). Mutants lacking theLHCs CP24, CP26, and CP29 were studied by picosecond fluorescence spectroscopy. Whereasthe lack of CP26 had little or no effect, the absence of CP29 or CP24 indicated that a large fractionof the LHCs were disconnected from the core complex. Plant PSII presents a major challenge forfuture research.

Excitation Transfer in Cyanobacterial Photosystem I Complexes

PSI is one of the most intricate chlorophyll–protein complexes in nature. Its unique light-harvesting and transfer requirements, together with its many interconnected subunits, have led toa very high degree of structural conservation (135). Approximately 90 chlorophylls have remainedlargely unchanged by the more than two billion years of evolution between Cyanobacterium andflowering plants (38, 77, 82). Consequently, excitation energy transfer studies in cyanobacterialPSI are relevant to the core of plant PSI, but the excitation transfer from LHCs to the core ismuch more complicated and may be unique to each organism. Early studies on excitation energytransfer in cyanobacterial PSI concentrated on the nature of the network of 96 chlorophylls, whichhave no apparent symmetry (117). This theoretical approach stressed the robustness of the systembut could not identify the specific function of individual chlorophylls or groups of chlorophylls.

Intraprotein excitation transfer may be coherent at the >1-ps timescale, and the trapping timewithin the cores of both PSI and PSII is very short (∼3 ps) (136). The respective trapping timeswith attached antennae, however, are much longer: 60–90 ps in PSI (137) and 300–500 ps in PSII.The longer trapping time in the complete photosystem, compared with that in the core, is due toa small extent to interprotein hopping and to a large extent to dilution of the exciton density inthe core by the many pigments surrounding the trap. It is an entropic effect. The dilution is morepronounced in PSII, which is a shallow trap, than in PSI, which is a deep trap. Some authors haveargued that trapping in PSII, which is approximately one-fourth as fast as that in PSI, requiresthat PSII and PSI be separated in grana and stroma lamellae in order for their turnover rates tobe balanced under weak illumination (136).

Experiments using the anisotropic pump-probe method and other ultrafast kinetic techniqueswith cyanobacterial PSI revealed excitation transfer as fast as 100 fs, which represents the fastestprocess of a single energy transfer step between two chlorophylls (see References 7 and 64 and


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references therein). Experiments performed at 77 K, where the absorbance spectrum and fluores-cence emission are sharper, revealed a few states of excitation transfer, equilibration, and trappingwithin the PSI complex. Excitation of the bulk antenna at 670 and 680 nm induced an energy trans-fer process that populates the chlorophyll a spectral form at 685 to 687 nm within a few transfersteps of 300 to 400 fs. Equilibration with the longest-wavelength-absorbing pigments occurswithin 4 to 6 ps, and energy equilibration processes involving low-energy chlorophylls participatein a 30–50-ps process of photochemical trapping for excitation by P700 (86). Time-resolved fluo-rescence emission measurements, performed at room temperature, revealed differences betweenthe equilibration components of 3.4 to 15 ps and differences between the trapping componentsof 23 to 50 ps (138, 139). It has been suggested that excitation energy is equilibrated with a life-time of 0.6 ps among the bulk chlorophylls, is distributed in 3 to 4 ps between the bulk and redchlorophylls, and is trapped in the RC within 19 ps (140). The presence of an additional LHC ineukaryotic PSI, operating without loss in quantum efficiency, demands even more sophisticatedstudies.

Excitation Transfer in Eukaryotic Photosystem I

The eukaryotic PSI complex is much larger and more complicated than its cyanobacterial counter-part. Algae and higher plants contain additional LHCs that increase the absorption cross section ofPSI. In higher plants, these LHCs are composed of two heterodimers: Lhca1–Lhca4 and Lhca2–Lhca3, which are organized as a crescent shape around the core (7, 64, 82, 141). Several specificproperties distinguish PSI from other photosynthetic complexes: (a) Its high chlorophyll densityrenders specific time-resolved studies of the ET processes in the RC more difficult, and (b) it haschlorophyll forms with lower energy than the RC chlorophylls, known as red chlorophylls. De-spite their low energy, red chlorophylls are supposed to be very important for the overall functionof PSI (7, 64). Time-resolved fluorescence measurements have been performed on isolated coreand intact PSI particles and stroma membranes from Arabidopsis thaliana to characterize the typeof energy-trapping kinetics in higher-plant PSI (142). No bottleneck in the energy flow from thebulk antenna compartments to the RC has been found. Both the core PSI and the full PSI were traplimited. The apparent charge-separation lifetime was ∼6 ps, which is faster than the trap limitationof 50 ps.

No red chlorophylls were found in the PSI core complex. Two red chlorophyll compoundslocated in the peripheral LHCs, with decay lifetimes of 33 and 95 ps, were observed in the intactPSI particles. The two red states have been tentatively attributed to the two light-harvestingcomplexes Lhca3 and Lhca4. The influence of the red chlorophylls on the slowing of the overalltrapping kinetics in the intact PSI complex was estimated to be approximately four times largerthan the effect of the bulk antenna enlargement. The fact that those experiments were carriedout at ambient temperature reinforces these conclusions. More recent research has investigatedthe role of the individual antenna complexes in excitation energy transfer and trapping in PSI ofhigher plants (143, 144).

Native PSI and subcomplexes with different antenna composition have been studied by pi-cosecond fluorescence spectroscopy. These studies showed that Lhca3 and Lhca4, which harborthe red chlorophyll forms, have similar emission spectra and that they transfer excitation energyto the core at a rate of ∼25 ns. In contrast, the energy transfer from Lhca1 and Lhca2, the blueantenna complexes, occurs about four times faster. Thus, the energy transfer from the Lhca1–Lhca4 and Lhca2–Lhca3 dimers to the core is faster than energy equilibration within these dimers.Moreover, all four monomers contribute almost equally to the transfer to the core, and the redforms decrease the overall trapping rate by approximately one-half. The excitation energy transfer

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Figure 8Pathways for excitation transfer in plant photosystem I. Coordinates are from Protein Data Bank entry3LW5. The protein chains and peripheral chlorophylls have been removed; only the porphyrin rings areshown. Core chlorophylls are in magenta, light-harvesting complex I (LHCI) in green, and quinones in blue.The Fx cluster is represented as orange and yellow spheres. The two circled groups of chlorophylls aresymmetrically organized in PsaA and PsaB, but their contribution to excitation transfer from LHCI is vastlydifferent. The arrows indicate the two main pathways for excitation transfer; the Lhca1 pathway is likely tobe dominant.

routes in PSI have been presented in detail (143, 144). Figure 8 depicts energy transfer andtrapping in plant PSI as presented in these studies, superimposed on a model highlighting thechlorophyll positions in the complex. The crystal structure of plant PSI identified three plausi-ble routes for excitation transfer from the LHCI complex to the core complex (52, 79, 82). Themost prominent one connects Lhca1 chlorophylls and chlorophylls coordinated by the core PsaB(Figure 8). The second route is between Lhca2 and PsaA, and the third, most elusive one is be-tween Lhca3 and PsaA. Similarly, light-harvesting measurements performed with the PSI–LHCIsupercomplex indicated the presence of two or three decay components. The fast one was ∼10 ps,which represented excitation equilibration between the bulk pigments and the redmost forms inthe core complex (7, 64). Two slower decay components of 18 to 24 ps and 60 to 100 ps wereattributed to direct trapping in the core and trapping following excitation in LHCI, respectively.The average lifetimes are similar to those obtained by modeling of excitation transfer in plant PSI(117). A recent detailed study showed that transfer from the blue Lhcas (Lhca1 and Lhca2) to thecore is very fast and occurs in ∼10 ps (144). These two complexes also transfer excitation to the redLhcas (Lhca3 and Lhca4) at a similar transfer rate. Lhca3 and Lhca4 can also transfer excitationdirectly to the core, but at a slower rate of ∼40 ps. This study concluded that in PSI the trappingtime is ∼50 ps and that most red forms are associated with LHCI. All Lhca chlorophylls transfer


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excitation energy to the core—Lhca1 and Lhca2 very rapidly and Lhca3 and Lhca4 somewhatmore slowly (64). Clearly, excitation transfer between the two Lhca dimers is very poor, and mostof the excitation transfer from the LHCI proceeds through Lhca1 and Lhca2, which are bluerand have higher energy levels. Apparently, excitation transfer from chlorophylls in the peripheryof PSI occurs via the paradoxical route of blue to red to blue in LHCI, then red to blue to P700in the core.

Red chlorophylls are present in the PSI of cyanobacteria and in the light-harvesting belt ofplant PSI. In cyanobacteria, red chlorophylls can affect the trapping kinetics of excitation energy, asshown by measurements performed in PSI from various species (139). All calculations of individualpigment energies are based on the high-resolution PSI structure from Thermosynechococcus elongatus,which contains a relatively large number of red pigments (53). The strength of the red absorptionvaries significantly between various cyanobacterial species; in particular, Synechocystis has very lowlevels of red chlorophylls in comparison to Thermosynechococcus (139). On the basis of ring-to-ring distances and dipole orientation, Jordan et al. (53) identified one chlorophyll trimer (B31–B32–B33) and three dimers (A32–B7, A38–A37, and B37–B38) as candidates for strongly coupledpigments in the RC. We crystallized and solved the structure of Synechocystis PSI and found that thering location and the local environment of dimer A38–A39 remained virtually unchanged betweenSynechocystis and Thermosynechococcus (58). The ring positions of the A32–B7 dimer shifted slightlyfrom Thermosynechococcus to Synechocystis, and the side chain coordinating the magnesium of B7changed from glutamine to histidine. These changes can contribute greatly to the Qy position ofthe pigment (126). The A32–B7 dimer may be sensitive to the oligomerization state of the complex,given that some red absorption is lost upon monomerization (139). In contrast, it is very clear thatchlorophyll b33 is completely missing from the stacked trimer observed in Thermosynechococcus. Inplant PSI, the corresponding chlorophyll has shifted substantially, which may cause the loss of redforms in the core complex (79, 82). One of the remaining dimers, either B37–B38 or B31–B32,may be responsible for the residual red absorbance observed in Synechocystis (58).

Due to the pseudosymmetry of PsaA and PsaB, cyanobacterial PSI and the core of plant PSIcontain another chlorophyll trimer (A20–A21–PL1) that is coordinated by PsaA. These sections ofPSI contain high chlorophyll concentrations, and they may represent the so-called red sections ofthe core complex. The excitation transfer from Lhca1 to P700 must go through the correspondingred section of PsaB (Figure 8). For symmetry reasons, it is likely that the corresponding sectionin PsaA has a similar role in excitation transfer. However, its position, in proximity to Lhca2and Lhca3, precludes direct excitation transfer between them. It is highly likely that the PsaAsymmetrical bundle of chlorophylls depicted in Figure 8 is functional in state transition and bindsLHCII in an almost identical fashion to the binding of Lhca1 by PsaB (58). This scenario suggeststhat LHCII monomers play an important role in state transition. Symmetrical sections of thePSI core may be directly involved in the final stage of excitation transfer from the antenna ofthe core to P700. Two critical chlorophyll molecules (X1140 and X1239) that are supposed totransfer the excitation energy directly to the electron transfer chain are symmetrically present inthese sections. The chlorophyll distribution in this area suggests that it is “blue.” If so, excitationtransfer from Lhca4 (red) goes through Lhca1 (blue), through the contact in PsaB (red) to P700,and finally through the connecting chlorophyll assembly (blue) to P700. Such a route is difficultto explain without assuming coherent excitation transfer among adjacent chlorophyll assemblies,regardless of the presence of the red inclination in some of them.

The most intriguing properties of plant PSI are that its chlorophyll concentration is ∼0.5 M, itscarotenoid concentration is ∼0.15 M, and it is able to avoid concentration quenching to keep thequantum efficiency close to one (52, 64, 68). The explanation for this may be hidden in the proteinstructure that, at least in the core, was highly conserved over more than 3.5 billion years of evolution

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(42, 47). Apparently, the proteins serve as a scaffold that keeps the pigments in the correct geometryto facilitate fast energy transfer and to prevent excited-state quenching. In addition, the proteinmust play a role in controlling the energy levels of the pigments. The tight structure of the proteinand the fine-tuning of the position of the amino acids and their side chains provide vibrationalenergy (phonons) for fine-tuning the energy levels of both individual pigments and a group ofpigments that form the excitation transfer moiety. Such quantum-mechanical consideration mayprovide a better explanation for the mechanism of excitation transfer than spectral deconvolutionattributed to individual pigments (125, 145). This arrangement allows energy transfer uphill anddownhill through the excited-state energy landscape and may allow a fresh look at the phenomenonof red chlorophylls. Three chlorophylls (B31, B32, and B33), identified in the crystal structure ofPSI from Thermosynechococcus elongatus, may form the long-wavelength red spectrum (53). This ideagained strong support with the observations that plant PSI B33 has moved significantly (38, 79, 82)and that B33 is lacking in Synechocystis PSI, as is the long “red” pigment (58). Thus, the red formwas attributed to B33. The lack of quantum losses at the physiological temperatures was explainedby thermal energy that fills the energetic gap between the red donor and the blue acceptor (146). At77 K, fluorescence loses energy when B33 creates an energy trap. However, B33 is in the peripheryof PSI, which limits its function in dissipating excess energy. In contrast, several theoretical andexperimental results suggest that the red form plays a major role in excitation transfer to P700(64). If we assume room-temperature conditions, coherent excitation transfer may provide analternative and more general explanation for the presence of the red form. According to this view,the red form may arise from an ambient-temperature quantum effect in a group of pigments. Thered form arose from the interaction between the pigments and the phonon, which has positiveeffects on excitation transfer. At low temperatures, the positive thermal energy dissipates, causingincreased fluorescence and energy loss.

Investigating quantum-mechanical effects on the red forms at various temperatures may providea wealth of information about excitation transfer in PSI. Experiments on 2DES and transientabsorption with PSI crystals may play a key role in unraveling the mechanism of excitation transferin large pigment–protein complexes.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We apologize to all the investigators whose work could not be cited in this review. N.N. thanksthe ESRF, SLS, and BESSY II synchrotrons for beam time and the staff scientists for excellentguidance and assistance. The writing of this review was supported by the European ResearchCouncil through grant 293579-HOPSEP, the Israel Science Foundation through grant 71/14,and the I-CORE Program of the Planning and Budgeting Committee and the Israel ScienceFoundation through grant 1775/12.

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BI84-FrontMatter ARI 24 April 2015 13:54

Annual Review ofBiochemistry

Volume 84, 2015ContentsIt Seems Like Only Yesterday

Charles C. Richardson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Veritas per structuramStephen C. Harrison � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �37

Nuclear OrganizationYosef Gruenbaum � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �61

The Balbiani Ring Story: Synthesis, Assembly, Processing, andTransport of Specific Messenger RNA–Protein ComplexesPetra Bjork and Lars Wieslander � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �65

Functions of Ribosomal Proteins in Assembly of EukaryoticRibosomes In VivoJesus de la Cruz, Katrin Karbstein, and John L. Woolford Jr. � � � � � � � � � � � � � � � � � � � � � � � � � � � � �93

Lamins: Nuclear Intermediate Filament Proteins with FundamentalFunctions in Nuclear Mechanics and Genome RegulationYosef Gruenbaum and Roland Foisner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 131

Regulation of Alternative Splicing Through Coupling withTranscription and Chromatin StructureShiran Naftelberg, Ignacio E. Schor, Gil Ast, and Alberto R. Kornblihtt � � � � � � � � � � � � � � � � 165

DNA Triplet Repeat Expansion and Mismatch RepairRavi R. Iyer, Anna Pluciennik, Marek Napierala, and Robert D. Wells � � � � � � � � � � � � � � � � 199

Nuclear ADP-Ribosylation and Its Role in Chromatin Plasticity,Cell Differentiation, and EpigeneticsMichael O. Hottiger � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 227

Application of the Protein Semisynthesis Strategy to the Generationof Modified ChromatinMatthew Holt and Tom Muir � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 265

Mechanisms and Regulation of Alternative Pre-mRNA SplicingYeon Lee and Donald C. Rio � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

The Clothes Make the mRNA: Past and Present Trendsin mRNP FashionGuramrit Singh, Gabriel Pratt, Gene W. Yeo, and Melissa J. Moore � � � � � � � � � � � � � � � � � � � 325

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Biochemical Properties and Biological Functions of FET ProteinsJacob C. Schwartz, Thomas R. Cech, and Roy R. Parker � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 355

Termination of Transcription of Short Noncoding RNAs by RNAPolymerase IIKaren M. Arndt and Daniel Reines � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 381

PIWI-Interacting RNA: Its Biogenesis and FunctionsYuka W. Iwasaki, Mikiko C. Siomi, and Haruhiko Siomi � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 405

The Biology of Proteostasis in Aging and DiseaseJohnathan Labbadia and Richard I. Morimoto � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 435

Magic Angle Spinning NMR of Proteins: High-Frequency DynamicNuclear Polarization and 1H DetectionYongchao Su, Loren Andreas, and Robert G. Griffin � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 465

Cryogenic Electron Microscopy and Single-Particle AnalysisDominika Elmlund and Hans Elmlund � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 499

Natural Photoreceptors as a Source of Fluorescent Proteins,Biosensors, and Optogenetic ToolsDaria M. Shcherbakova, Anton A. Shemetov, Andrii A. Kaberniuk,

and Vladislav V. Verkhusha � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 519

Structure, Dynamics, Assembly, and Evolution of Protein ComplexesJoseph A. Marsh and Sarah A. Teichmann � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 551

Mechanisms of Methicillin Resistance in Staphylococcus aureusSharon J. Peacock and Gavin K. Paterson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 577

Structural Biology of Bacterial Type IV Secretion SystemsVidya Chandran Darbari and Gabriel Waksman � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 603

ATP SynthaseWolfgang Junge and Nathan Nelson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 631

Structure and Energy Transfer in Photosystems of OxygenicPhotosynthesisNathan Nelson and Wolfgang Junge � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 659

Gating Mechanisms of Voltage-Gated Proton ChannelsYasushi Okamura, Yuichiro Fujiwara, and Souhei Sakata � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 685

Mechanisms of ATM ActivationTanya T. Paull � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 711

A Structural Perspective on the Regulation of the Epidermal GrowthFactor ReceptorErika Kovacs, Julie Anne Zorn, Yongjian Huang, Tiago Barros, and John Kuriyan � � � 739

vi Contents

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Chemical Approaches to Discovery and Study of Sources and Targetsof Hydrogen Peroxide Redox Signaling Through NADPH OxidaseProteinsThomas F. Brewer, Francisco J. Garcia, Carl S. Onak, Kate S. Carroll,

and Christopher J. Chang � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 765

Form Follows Function: The Importance of EndoplasmicReticulum ShapeL.M. Westrate, J.E. Lee, W.A. Prinz, and G.K. Voeltz � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 791

Protein Export into Malaria Parasite–Infected Erythrocytes:Mechanisms and Functional ConsequencesNatalie J. Spillman, Josh R. Beck, and Daniel E. Goldberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 813

The Twin-Arginine Protein Translocation PathwayBen C. Berks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 843

Transport of SugarsLi-Qing Chen, Lily S. Cheung, Liang Feng, Widmar Tanner,

and Wolf B. Frommer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 865

A Molecular Description of Cellulose BiosynthesisJoshua T. McNamara, Jacob L.W. Morgan, and Jochen Zimmer � � � � � � � � � � � � � � � � � � � � � � � 895

Cellulose Degradation by Polysaccharide MonooxygenasesWilliam T. Beeson, Van V. Vu, Elise A. Span, Christopher M. Phillips,

and Michael A. Marletta � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 923

Physiology, Biomechanics, and Biomimetics of Hagfish SlimeDouglas S. Fudge, Sarah Schorno, and Shannon Ferraro � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 947

Indexes

Cumulative Index of Contributing Authors, Volumes 80–84 � � � � � � � � � � � � � � � � � � � � � � � � � � � 969

Cumulative Index of Article Titles, Volumes 80–84 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 973

Errata

An online log of corrections to Annual Review of Biochemistry articles may be found athttp://www.annualreviews.org/errata/biochem

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structure and energy transfer in photosystems of oxygenic … · 2015-06-26 ·...

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