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Biogenesis of the Cyanobacterial Thylakoid Membrane System An MINIREVIEW Biogenesis ofthe cyanobacterial thylakoid membrane system ^ an update Jorg¨ Nickelsen1, Birgit Rengstl1, Anna Stengel1, Marco Schottkowski1,Jurgen¨ Soll2 & Elisabeth Ankele2 1Molekulare Pflanzenwissenschaften, Biozentrum LMU M ¨unchen, Planegg-Martinsried, Germany; and 2Biochemie und Physiologie der Pflanzen, Biozentrum LMU M ¨unchen,Planegg-Martinsried, Germany Downloaded from https://academic.oup.com/femsle/article/315/1/1/540911 by guest on 02 October 2021 Correspondence: Jorg¨ Nickelsen, Abstract Molekulare Pflanzenwissenschaften, Biozentrum LMU Munchen, ¨ Großhaderner Current molecular analyses suggest that initial steps of the biogenesis of cyano- Str. 2-4, 82152 Planegg-Martinsried, bacterial photosystems progress in a membrane subfraction representing a Germany. Tel.: 10049 89 2180 74773; fax: biosynthetic center with contact to both plasma and thylakoid membranes. This 10049 89 2180 997 4773; e-mail: special membrane fraction is defined by the presence of the photosystem II [email protected] assembly factor PratA. The proposed model suggests that both biogenesis of protein complexes and insertion of chlorophyll molecules into the photosystems Received 7 July 2010; revised 30 July 2010; occur in this intermediate membrane system. accepted 2 August 2010. Final version published online 10 September 2010. DOI:10.1111/j.1574-6968.2010.02096.x Editor: Hermann Heipieper Keywords Synechocystis; membrane biogenesis; photosystem II; PratA; Pitt. scenarios can be envisioned. (1) Protein, lipid and pigment Introduction synthesis occurs directly on pre-existing TMs. (2) The Cyanobacteria represent the phylogenetic ancestors of chlo- components are synthesized and assembled in specialized roplasts from present-day plants and, similar to those, they thylakoid regions. (3) Initial production of polypeptides and contain three major differentiated membrane systems. These assembly of protein/pigment complexes occur at the PM, include the outer membrane and the inner or plasma and these precomplexes are transferred to the thylakoids via membrane (PM), which, together with the intervening an unknown way (Fig. 1). periplasm and the peptidoglycan layer, form the cellular Scenario 1 appears rather unlikely, because ultrastructural envelope. Interior to the PM is the thylakoid membrane cryo-electron microscopy data clearly show that TM layers are (TM) system representing the site of the photosynthetic essentially devoid of ribosomes (van de Meene et al., 2006). light reactions coupled to ATP and NADPH generation. All This suggests that protein synthesis, and thus biogenesis, does three membrane systems differ from one another with not occur in direct association with the photosynthetically regard to their pigment, lipid and protein composition active thylakoids. However, ribosome clusters are observed (Norling et al., 1998; Wada & Murata, 1998). This observa- close to the PM and near TM structures that extend into the tion provokes the following questions: Where is TM synth- central cytoplasm, favoring models 2 and/or 3 (van de Meene esis initiated in cyanobacteria? How is specificity between et al., 2006). Furthermore, TMs appear to converge on the the different membranes achieved and maintained? And PM at specific sites (Fig. 2). These convergence sites have been how are these processes organized at the molecular level? speculated to eventually mark so-called thylakoid centers, MICROBIOLOGY LETTERS MICROBIOLOGY Two excellent reviews have recently summarized the possible where TM biogenesis is initiated (van de Meene et al., 2006). models and key questions of TM biogenesis, which are It is still under debate whether at these regions permanent or controversially discussed (Liberton & Pakrasi, 2008; Mulli- transient fusions between PM and TM occur. If so, these neaux, 2008 and references therein). In brief, three different would allow the transfer of lipids and proteins to the FEMS Microbiol Lett 315 (2011) 1–5 c 2010 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved 2 J. Nickelsen et al. developing TM resembling the situation found in purple convergence sites marking a membrane subfraction with bacteria such as Rhodospirillum rubrum (Collins & Remsen, contact to both the PM and the TM. These sites possibly 1991; Liberton et al., 2006; van de Meene et al., 2006). represent the regions at which protein/pigment complexes are Here, we aim at incorporating some very recent findings of assembled and incorporated into photosynthetic membranes. membrane fractionation studies of the model organism Synechocystis sp. PCC 6803 (hereafter Synechocystis 6803) Protein synthesis/assembly into the various abovementioned scenarios. We propose a novel working model combining scenarios 2 and 3 with TM Three major membrane complexes constitute the basic apparatus of TMs mediating photosynthetic electron flow, i.e. photosystem II (PSII), the cytochrome b6f complex and photosystem I (PSI). PSII functions as a water-plastoqui- none oxidoreductase which, in cyanobacteria, consists of 20 Downloaded from https://academic.oup.com/femsle/article/315/1/1/540911 by guest on 02 October 2021 protein subunits, 35 chlorophyll a (chl a) molecules and several additional cofactors including the manganese cluster catalyzing photosynthetic water splitting (Nelson & Ben- Shem, 2004). PSI comprises only 12 subunits, approximately 80 chlorophylls as well as Fe–S clusters and phylloquinones (Nelson & Ben-Shem, 2004). While the structures of these molecular machines have recently been well established (Stroebel et al., 2003; Ferreira et al., 2004; Loll et al., 2005; Amunts et al., 2007), to date, only limited information is available on the molecular details of their biogenesis (Nixon et al., 2010). Earlier work based on membrane fractionation studies initially suggested that precomplexes of both photosystems are assembled within the PM and not the TM in the cyanobacterium Synechocystis 6803 (Zak et al., 2001). Using a combination of sucrose density centrifugation and aqu- eous two-phase partitioning, protein components of the core reaction center of PSII (D1, D2, Cyt b559) as well as of PSI (PsaA and PsaB), were identified in the PM, whereas more extrinsic proteins such as the inner antenna protein CP47 of PSII were found in TM preparations only. In addition, PSII biogenesis factors, such as the D1 C-terminal protease CtpA or the PSI assembly factors Ycf3 and Ycf4, Fig. 1. Models for TM biogenesis. Synthesis and assembly of photo- were mainly or exclusively detected in the PM (Zak et al., system components occur on (a) pre-existing thylakoids or (b) in specialized TMs (STM). Alternatively, the PM represents the site of early 2001). Together with the finding that the PM-localized core photosystem biogenesis steps (c), subsequently precomplexes are trans- complexes contain chlorophyll molecules and can perform ported to the TM via (1) transient connecting regions or (2) vesicle single light-induced charge separations, these data strongly transport. suggest that the photosystem core complexes found in the Fig. 2. Ultrastructure of Synechocystis 6803. Electron micrographs of a Synechocystis 6803 cell (A, scale bar = 200 nm). Sites of TM convergence are shown at higher magnification (a, scale bar = 100 nm). c 2010 Federation of European Microbiological Societies FEMS Microbiol Lett 315 (2011) 1–5 Published by Blackwell Publishing Ltd. All rights reserved Cyanobacterial thylakoid membrane biogenesis 3 PM, or a specialized section of it, exist in a preassembled acke & Zerges, 2007). This might indicate an evolutionary state (Keren et al., 2005; Srivastava et al., 2006). conservation of the molecular principles that underlie TM Further support for the idea that at least PSII biogenesis biogenesis. begins at non-TM sites was obtained during analysis of the PratA protein from Synechocystis 6803 (Klinkert et al., 2004). PratA consists of nine consecutive tetratricopeptide repeat Chlorophyll synthesis (TPR) units, a motif that is known to mediate protein–pro- Photosynthesis requires the absorption of light, which is tein interactions. Thereby, it could form a bridge connecting mediated by photoactive pigments, for example chloro- multiple proteins and serve as a scaffold factor for correct phylls. In chloroplasts of Arabidopsis thaliana, the synthesis assembly of PSII (Schottkowski et al., 2009a). PratA directly of chlorophyll was described to occur in several plastidic interacts with the C-terminus of the D1 reaction center subcompartments (Eckhardt et al., 2004). While early steps protein of PSII, and its inactivation affects the C-terminal Downloaded from https://academic.oup.com/femsle/article/315/1/1/540911 by guest on 02 October 2021 in synthesis, i.e. the conversion of glutamate to 5-aminole- processing of D1, an early step of PSII biogenesis. This D1 vulinic acid, occur in the chloroplast stroma, the enzymes maturation occurs in almost all photosynthetic organisms, required for later steps are associated with the inner and it is required for the subsequent docking of the subunits envelope membrane or the TM (Fig. 3). These membrane- of the oxygen-evolving complex to the lumenal side of PSII. attached enzymes include the NADPH-protochlorophyllide Most intriguingly, PratA was shown to be a soluble protein oxidoreductase (POR) and the chlorophyll synthase (CS), located in the periplasm, which forms part of a 200 kDa which catalyze the reduction of protochlorophyllide a complex of an as yet unknown composition
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