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Conservation of Core Complex Subunits Shaped the Structure And University of Groningen Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana Alboresi, Alessandro; Le Quiniou, Clotilde; Yadav, Sathish K N; Scholz, Martin; Meneghesso, Andrea; Gerotto, Caterina; Simionato, Diana; Hippler, Michael; Boekema, Egbert J.; Croce, Roberta Published in: New Phytologist DOI: 10.1111/nph.14156 IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 2017 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Alboresi, A., Le Quiniou, C., Yadav, S. K. N., Scholz, M., Meneghesso, A., Gerotto, C., ... Morosinotto, T. (2017). Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana. New Phytologist, 213, 714-726. [nph.14156]. https://doi.org/10.1111/nph.14156 Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 12-11-2019 Research Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga Nannochloropsis gaditana Alessandro Alboresi1*, Clotilde Le Quiniou2*, Sathish K. N. Yadav3*, Martin Scholz4, Andrea Meneghesso1, Caterina Gerotto1, Diana Simionato1, Michael Hippler4, Egbert J. Boekema3, Roberta Croce2 and Tomas Morosinotto1 1Dipartimento di Biologia, Universita di Padova, Via U. Bassi 58/B, 35121 Padova, Italy; 2Department of Physics and Astronomy and Institute for Lasers, Life and Biophotonics, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV, Amsterdam, the Netherlands; 3Electron Microscopy Group, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Nijenborgh 7, 9747 AG Groningen, the Netherlands; 4Institute of Plant Biology and Biotechnology, University of Munster,€ Munster€ 48143, Germany Summary Author for correspondence: Photosystem I (PSI) is a pigment protein complex catalyzing the light-driven electron trans- Tomas Morosinotto port from plastocyanin to ferredoxin in oxygenic photosynthetic organisms. Several PSI sub- Tel: +39 0498277484 units are highly conserved in cyanobacteria, algae and plants, whereas others are distributed Email: [email protected] differentially in the various organisms. Received: 30 May 2016 Here we characterized the structural and functional properties of PSI purified from the Accepted: 13 July 2016 heterokont alga Nannochloropsis gaditana, showing that it is organized as a supercomplex including a core complex and an outer antenna, as in plants and other eukaryotic algae. New Phytologist (2017) 213: 714–726 Differently from all known organisms, the N. gaditana PSI supercomplex contains five doi: 10.1111/nph.14156 peripheral antenna proteins, identified by proteome analysis as type-R light-harvesting com- plexes (LHCr4-8). Two antenna subunits are bound in a conserved position, as in PSI in plants, Key words: electron microscopy, whereas three additional antennae are associated with the core on the other side. This peculiar Heterokonta, Light-harvesting complex, antenna association correlates with the presence of PsaF/J and the absence of PsaH, G and K Nannochloropsis, photosynthesis, photosyn- in the N. gaditana genome and proteome. thetic apparatus, photosystem. Excitation energy transfer in the supercomplex is highly efficient, leading to a very high trapping efficiency as observed in all other PSI eukaryotes, showing that although the supramolecular organization of PSI changed during evolution, fundamental functional proper- ties such as trapping efficiency were maintained. 2009; Busch & Hippler, 2011) where they serve as docking site Introduction for the association of the peripheral antenna (Lunde et al., 2000; In organisms performing oxygenic photosynthesis, Photosystem I Ben-Shem et al., 2003). (PSI) is responsible for the light-driven electron transport from The peripheral antenna is composed of light-harvesting com- plastocyanin/cytochrome 6 to ferredoxin (Raven et al., 1999; plexes (LHC) whose sequences vary in different organisms: Nelson & Yocum, 2006; Croce & van Amerongen, 2013; LHCa1–6 are present in plants (Jansson, 1999), LHCa1–9 are Bernal-Bayard et al., 2015). In eukaryotes, PSI is organized as a present in the green alga Chlamydomonas reinhardtii (Mozzo supercomplex composed of two moieties, the core and the et al., 2010), whereas LHCR proteins are believed to comprise peripheral antenna system. The PSI core is composed of 12–14 the peripheral antenna in red algae and diatoms (Busch et al., subunits (Busch & Hippler, 2011). PsaA and PsaB bind the reac- 2010; Busch & Hippler, 2011; Thangaraj et al., 2011). The num- tion center P700 as well as most of the cofactors involved in elec- ber of LHC associated with PSI is also variable: four subunits are tron transport and c. 100 chlorophylls (Chls) active in light associated with the PSI core in higher plants, in the moss harvesting (Jordan et al., 2001; Qin et al., 2015). PsaA and PsaB Physcomitrella patens, and in some red algae and diatoms (Ben- are highly conserved in cyanobacteria, algae and plants (Allen Shem et al., 2003; Veith & Buchel,€ 2007; Busch et al., 2010, et al., 2011). Other core subunits are instead differently dis- 2013). Differently, nine antenna subunits are found associated tributed in various phylogenetic groups. For instance PsaG and with PSI in other red algae (Gardian et al., 2007; Thangaraj et al., PsaH are only found in plants and green algae (Vanselow et al., 2011) as in the green alga C. reinhardtii (Drop et al., 2011). Finally, the oligomeric state of PSI also varies in different *These authors contributed equally to this work. organisms. Cyanobacterial PSI often has been reported to be a 714 New Phytologist (2017) 213: 714–726 Ó 2016 The Authors www.newphytologist.com New Phytologist Ó 2016 New Phytologist Trust This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. New Phytologist Research 715 trimer (Boekema et al., 1987; Jordan et al., 2001), although PSI Thylakoid solubilization and PSI isolation tetramers have been identified in a growing number of species (Watanabe et al., 2011, 2014; Li et al., 2014). However, PSI was Thylakoid membranes (corresponding to 500 lg of Chl) were found to be monomeric in all eukaryotes analyzed so far, includ- solubilized with 0.6% a-DM or 1% b-DM as described in (Basso ing plants (Ben-Shem et al., 2003; Kouril et al., 2005a), diatoms et al., 2014) and then fractionated by ultracentrifugation in a (Veith & Buchel,€ 2007; Ikeda et al., 2013), green and red algae 0.1–1 M sucrose gradient containing 0.06% a-DM and 10 mM (Gardian et al., 2007; Drop et al., 2011). HEPES (pH 7.5) (280 000 g,18h,4°C). Fractions of the sucrose A peculiar feature of PSI is the presence of Chls absorbing at gradient were then harvested with a syringe. PSI samples isolated energy lower than the primary electron donor P700, called red after a-DM or b-DM solubilization were named PSI-LHCa and forms (Croce & van Amerongen, 2013). Although these far red- PSI-LHCb, respectively. absorbing Chls account only for a small fraction of the total absorption, they have a strong influence in excitation energy Electron microscopy and image analysis transfer and trapping, slowing down the trapping time as they introduce uphill steps in the energy transfer process (Gobets Four microliters of purified sample was absorbed onto glow dis- et al., 2001; Jennings et al., 2003; Engelmann et al., 2006; Wient- charged carbon-coated grids and subsequently stained with 2% jes et al., 2011b). The presence of low energy absorbing Chls is uranyl acetate for contrast. Imaging was performed on a Tecnai ubiquitous in PSI, but their energy appears to be highly species- T20 equipped with a LaB6 tip operating at 200 kV. The dependent (Gobets & van Grondelle, 2001; Croce & van ‘GRACE’ system for semi-automated specimen selection and Amerongen, 2013). In plants, most red forms are associated with data acquisition (Oostergetel et al., 1998) was used to record the outer antenna complexes and in particular with LHCA3 and 2048 9 2048 pixel images at 9133 000 magnifications using a LHCA4 (Schmid et al., 1997; Castelletti et al., 2003), although Gatan 4000 SP 4K slow-scan CCD camera with a pixel size of the core also contains low energy forms (Croce et al., 1998; 0.224 nm. Three hundred thousand particles were picked from Gobets & van Grondelle, 2001). 16 000 raw images and single particles were analyzed with XMIPP In the present work, we investigated the structural and func- software (including alignments, statistical
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