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Photosynthetic Light-Harvesting (Antenna) Complexes—Structures and Functions

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Photosynthetic Light-Harvesting (Antenna) Complexes—Structures and Functions molecules Review Photosynthetic Light-Harvesting (Antenna) Complexes—Structures and Functions Heiko Lokstein 1,* , Gernot Renger 2,† and Jan P. Götze 3 1 Department of Chemical Physics and Optics, Charles University, Ke Karlovu 3, 12116 Prague, Czech Republic 2 Max-Volmer-Laboratorium, Technische Universität Berlin, Straße des 17. Juni 135, D-10623 Berlin, Germany 3 Institut für Chemie und Biochemie, Freie Universität Berlin, Arnimallee 22, D-14195 Berlin, Germany; [email protected] * Correspondence: [email protected] † Sadly, Professor Dr. Gernot Renger passed away on 12 January 2013. This article is dedicated to commemorate the outstanding contributions of Gernot Renger to oxygenic photosynthesis research. Abstract: Chlorophylls and bacteriochlorophylls, together with carotenoids, serve, noncovalently bound to specific apoproteins, as principal light-harvesting and energy-transforming pigments in photosynthetic organisms. In recent years, enormous progress has been achieved in the elucidation of structures and functions of light-harvesting (antenna) complexes, photosynthetic reaction centers and even entire photosystems. It is becoming increasingly clear that light-harvesting complexes not only serve to enlarge the absorption cross sections of the respective reaction centers but are vitally important in short- and long-term adaptation of the photosynthetic apparatus and regulation of the energy-transforming processes in response to external and internal conditions. Thus, the wide variety of structural diversity in photosynthetic antenna “designs” becomes conceivable. It is, however, common for LHCs to form trimeric (or multiples thereof) structures. We propose a simple, tentative explanation of the trimer issue, based on the 2D world created by photosynthetic membrane systems. Citation: Lokstein, H.; Renger, G.; Götze, J.P. Photosynthetic Keywords: bacteriochlorophylls; chlorophylls; carotenoids; excitation energy transfer; light-harvesting Light-Harvesting (Antenna) complexes; photosynthesis; pigment-protein complexes; photosystems; photoprotection Complexes—Structures and Functions. Molecules 2021, 26, 3378. https://doi.org/10.3390/ molecules26113378 1. Introduction Academic Editor: Leszek Fiedor (Bacterio)chlorophylls, (B)Chls, being noncovalently bound to specific apoproteins, are the major chromophores of most light-harvesting (antenna) complexes (LHCs). More- Received: 27 January 2021 over, together with metal-free (bacterio)pheophytins, (B)Pheo, (B)Chls are the principle Accepted: 28 May 2021 photochemically active pigments in photosynthetic organisms. Excitation arriving at the Published: 3 June 2021 lowest singlet excited state (S1) of special (B)Chls in the photochemical reaction centers (RCs) eventually leads to primary charge separation, thus converting light energy into Publisher’s Note: MDPI stays neutral electrochemical energy, ultimately providing the driving force for all processes in photo- with regard to jurisdictional claims in synthetic (and also heterotrophic) organisms [1]. The vast majority of (B)Chls, however, published maps and institutional affil- act as (accessory) light-harvesting pigments, increasing the optical cross sections of the iations. photochemical RCs by about two orders of magnitude and more [2]. (B)Chls are essential constituents of the RCs and account for the majority of the antenna pigments in nonoxygen-evolving (anoxygenic) photosynthetic bacteria. In all oxygen-evolving photosynthetic organisms, Chls a functions as a primary electron donor in Copyright: © 2021 by the authors. the RCs of both photosystems I and II (PSI and PSII). Moreover, a Chl a is also the primary Licensee MDPI, Basel, Switzerland. electron acceptor in PSI. An exception may be the cyanobacterium Acaryochloris (A.) marina, This article is an open access article in which Chl d also appears to be involved in electron transfer [3]. In higher plants and distributed under the terms and green algae, Chls a and b serve as the major antenna pigments in the LHCs. Chl b is found conditions of the Creative Commons only in the LHCs of higher plants and green algae, with most Chl b bound to the main light- Attribution (CC BY) license (https:// harvesting complex (LHCII). Chls a and b, and in some species also divinyl-Chls a and b, are creativecommons.org/licenses/by/ bound to the “prochlorophyte” (certain clades of the cyanobacterial radiation now better 4.0/). Molecules 2021, 26, 3378. https://doi.org/10.3390/molecules26113378 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 25 marina, in which Chl d also appears to be involved in electron transfer [3]. In higher plants and green algae, Chls a and b serve as the major antenna pigments in the LHCs. Chl b is found only in the LHCs of higher plants and green algae, with most Chl b bound to the Molecules 2021, 26, 3378 main light-harvesting complex (LHCII). Chls a and b, and in some species also 2divi- of 24 nyl-Chls a and b, are bound to the “prochlorophyte” (certain clades of the cyanobacterial radiation now better termed oxychlorobacteria) Chl-binding antenna complexes (Pcbs) termed[4]. Chls oxychlorobacteria) c are found in LHCs Chl-binding of different antenna algal clades complexes [5]. Chl (Pcbs) d and [4]. the Chls recentlyc are found discov- in LHCsered Chl of differentf [6] are found algal clades only in [5 ].certain Chl d andcyanobacteria. the recently Chl discovered d is the dominant Chl f [6] are pigment found onlyin A. inmarina certain [7,8] cyanobacteria.. The considerably Chl d is redshifted the dominant-absorbing pigment Chl in A. f marinawas first[7, 8discovered]. The considerably in stro- redshifted-absorbingmatolite-forming cyanobacteria Chl f was first [6]. discoveredThe synthesis in stromatolite-forming of Chl f and alternative cyanobacteria Chl-binding [6]. Theproteins synthesis seems of to Chl bef anda specific alternative response Chl-binding of certain proteins cyanobacteria seems to to be grow a specific under response far-red oflight certain conditions cyanobacteria [9]. Whether to grow Chl under f is also far-red involved light in conditions electron transfer, [9]. Whether or only Chl servesf is also as involvedan accessory in electron light-harvesting transfer, orpigment only serves, is currently as an accessory debated (e.g., light-harvesting [10,11]). pigment, is currentlyIn add debatedition to (e.g., (B)Chls, [10,11 most]). photosynthetic LHCs also bind carotenoids. In plants and Inalgae, addition LHCs to exclusively (B)Chls, most bind photosynthetic xanthophylls LHCs (oxygen also-containing bind carotenoids. derivatives In plants of caro- and algae,tenes). LHCs Bacterial exclusively LHCs and bind cyanobacterial, xanthophylls (oxygen-containing algal and plant core derivatives-antenna complexes of carotenes). of Bacterialboth PSI LHCsand II and can cyanobacterial, contain both carotenes algal and plantand their core-antenna oxygen derivatives. complexes of The both functions PSI and IIand can photophysics contain both carotenesof carotenoids and their (also oxygen when derivatives.bound to LHCs) The functions have been and covered photophysics exten- ofsively carotenoids in a previous (also when review bound [12]. toCarotenoids LHCs) have have been unique covered photophysical extensively infeatures a previous that reviewrender [their12]. Carotenoids spectroscopic have investigation, unique photophysical in particular features in LHCs, that render rather theirdifficult. spectroscopic Conven- investigation,tionally, carotenoid in particular excited in states LHCs, are rather assigned difficult. due Conventionally,to an assumed carotenoidC2h symmetry excited (in statesanalogy are to assigned linear polyenes). due to an However, assumed very C2h recent symmetry studies (in analogyhave suggested to linear that polyenes). the un- However,derlying ass veryumptions recent studiesmay not have apply suggested to carotenoids, that the in underlying particular to assumptions the optically may “dark” not applyfirst excited to carotenoids, singlet state in particular (S1) [13]. to the optically “dark” first excited singlet state (S1)[13]. StructuresStructures ofof ChlChl aa andand violaxanthinviolaxanthin (as(as representativesrepresentatives ofof theirtheir moleculemolecule classes),classes), asas wellwell asas thethe correspondingcorresponding absorptionabsorption spectraspectra andand energyenergy levels,levels, areare shownshown inin FigureFigure1 .1. In In spitespite ofof thethe vastvast taxonomictaxonomic diversitydiversity ofof photosyntheticphotosynthetic organisms,organisms, thethe mechanismsmechanisms ofof thethe primaryprimary photochemicalphotochemical reactions reactions performed performed by by (B)Chls (B)Chls and and the the other other associated associated cofactors cofac- intors the in RCs the areRCs very are very similar, similar, while—in while marked—in mar contrast—bothked contrast—both the structures the structures of LHCs of LHCs and theand bound the bound pigments pigments exhibit exhibit a remarkable a remarkable variety. variety. FigureFigure 1.1.Molecular Molecular structures structures and and absorption absorption spectra spectra of of chlorophyll chlorophylla ( lefta (left) and) and the the carotenoid carotenoid (xanthophyll) (xanthophyll) violaxanthin violaxan- (thinright ()right as representatives) as representatives of their of respectivetheir respective molecule molecule classes, classes as well, as aswell the as corresponding the corresponding energy energy level schemes.level
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