PSI of the Colonial Alga Botryococcus braunii Has an Unusually Large Antenna Size
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33051267
PubMed Central
PMC7723122
DOI
10.1104/pp.20.00823
PII: pp.20.00823
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis chemie ultrastruktura MeSH
- Chlamydomonas reinhardtii chemie ultrastruktura MeSH
- konformace proteinů MeSH
- molekulární modely MeSH
- podjednotky proteinů MeSH
- světlosběrné proteinové komplexy chemie ultrastruktura MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- podjednotky proteinů MeSH
- světlosběrné proteinové komplexy MeSH
PSI is an essential component of the photosynthetic apparatus of oxygenic photosynthesis. While most of its subunits are conserved, recent data have shown that the arrangement of the light-harvesting complexes I (LHCIs) differs substantially in different organisms. Here we studied the PSI-LHCI supercomplex of Botryococccus braunii, a colonial green alga with potential for lipid and sugar production, using functional analysis and single-particle electron microscopy of the isolated PSI-LHCI supercomplexes complemented by time-resolved fluorescence spectroscopy in vivo. We established that the largest purified PSI-LHCI supercomplex contains 10 LHCIs (∼240 chlorophylls). However, electron microscopy showed heterogeneity in the particles and a total of 13 unique binding sites for the LHCIs around the PSI core. Time-resolved fluorescence spectroscopy indicated that the PSI antenna size in vivo is even larger than that of the purified complex. Based on the comparison of the known PSI structures, we propose that PSI in B. braunii can bind LHCIs at all known positions surrounding the core. This organization maximizes the antenna size while maintaining fast excitation energy transfer, and thus high trapping efficiency, within the complex.
Zobrazit více v PubMed
Alboresi A, Le Quiniou C, Yadav SKN, Scholz M, Meneghesso A, Gerotto C, Simionato D, Hippler M, Boekema EJ, Croce R, et al. (2017) Conservation of core complex subunits shaped the structure and function of photosystem I in the secondary endosymbiont alga PubMed PMC
Anderson JM, Chow WS, Park YI(1995) The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46: 129–139 PubMed
Ballottari M, Dall’Osto L, Morosinotto T, Bassi R(2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282: 8947–8958 PubMed
Beardall J, Allen D, Bragg J, Finkel ZV, Flynn KJ, Quigg A, Rees TAV, Richardson A, Raven JA(2009) Allometry and stoichiometry of unicellular, colonial and multicellular phytoplankton. New Phytol 181: 295–309 PubMed
Benson SL, Maheswaran P, Ware MA, Hunter CN, Horton P, Jansson S, Ruban AV, Johnson MP(2015) An intact light harvesting complex I antenna system is required for complete state transitions in PubMed
Bos I, Bland KM, Tian L, Croce R, Frankel LK, Amerongen H Van, Bricker TM, Wientjes E (2017) Multiple LHCII antennae can transfer energy ef fi ciently to a single photosystem I. Biochimt Biophys Acta 1858: 371–378 PubMed
Browne DR, Jenkins J, Schmutz J, Shu S, Barry K, Grimwood J, Chiniquy J, Sharma A, Niehaus TD, Weiss TL, et al. (2017) Draft nuclear genome sequence of the liquid hydrocarbon-accumulating green microalga PubMed PMC
Busch A, Hippler M(2011) The structure and function of eukaryotic photosystem I. Biochim Biophys Acta 1807: 864–877 PubMed
Carbonera D, Agostini G, Morosinotto T, Bassi R(2005) Quenching of chlorophyll triplet states by carotenoids in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. Biochemistry 44: 8337–8346 PubMed
Chukhutsina VU, Holzwarth AR, Croce R (2019) Time-resolved fluorescence measurements on leaves: Principles and recent developments. Photosynth Res 140: 355–369 PubMed PMC
Chukhutsina VU, Liu X, Xu P, Croce R(2020) Light-harvesting complex II is an antenna of photosystem I in dark-adapted plants. Nat Plants 6: 860–868 PubMed
Croce R, Morosinotto T, Castelletti S, Breton J, Bassi R(2002) The Lhca antenna complexes of higher plants photosystem I. Biochim Biophys Acta 1556: 29–40 PubMed
Croce R, van Amerongen H(2020) Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy. Science 369: eaay2058. PubMed
Croce R, van Amerongen H(2013) Light-harvesting in photosystem I. Photosynth Res 116: 153–166 PubMed PMC
de la Rosa-Trevín JM, Quintana A, Del Cano L, Zaldívar A, Foche I, Gutiérrez J, Gómez-Blanco J, Burguet-Castell J, Cuenca-Alba J, Abrishami V, et al. (2016) Scipion: A software framework toward integration, reproducibility and validation in 3D electron microscopy. J Struct Biol 195: 93–99 PubMed
Drop B, Webber-Birungi M, Fusetti F, Kouřil R, Redding KE, Boekema EJ, Croce R(2011) Photosystem I of PubMed PMC
Drop B, Yadav K N S, Boekema EJ, Croce R(2014) Consequences of state transitions on the structural and functional organization of photosystem I in the green alga PubMed
Engelmann E, Zucchelli G, Casazza AP, Brogioli D, Garlaschi FM, Jennings RC(2006) Influence of the photosystem I-light harvesting complex I antenna domains on fluorescence decay. Biochemistry 45: 6947–6955 PubMed
Eroglu E, Okada S, Melis A(2011) Hydrocarbon productivities in different PubMed PMC
García-Cubero R, Cabanelas ITD, Sijtsma L, Kleinegris DMM, Barbosa MJ(2018) Production of exopolysaccharide by
Gobets B, Kennis JTM, Ihalainen JA, Brazzoli M, Croce R, Van Stokkum IHM, Bassi R, Dekker JP, Van Amerongen H, Fleming GR, et al. (2001) Excitation energy transfer in dimeric light harvesting complex I: A combined streak-camera/fluorescence upconversion study. J Phys Chem B 105: 10132–10139
Gouveia JD, Ruiz J, van den Broek LAM, Hesselink T, Peters S, Kleinegris DMM, Smith AG, van der Veen D, Barbosa MJ, Wijffels RH(2017) PubMed
Grotjohann I, Fromme P(2013) Photosystem I In Lennarz W, and Lane M, eds, Ed 2 Encyclopedia of Biological Chemistry, New York, pp 503–507
Iwai M, Grob P, Iavarone AT, Nogales E, Niyogi KK(2018) A unique supramolecular organization of photosystem I in the moss PubMed PMC
Iwai M, Yokono M(2017) Light-harvesting antenna complexes in the moss PubMed
Järvi S, Suorsa M, Paakkarinen V, Aro E-M(2011) Optimized native gel systems for separation of thylakoid protein complexes: Novel super- and mega-complexes. Biochem J 439: 207–214 PubMed
Jennings RC, Zucchelli G, Croce R, Garlaschi FM(2003) The photochemical trapping rate from red spectral states in PSI-LHCI is determined by thermal activation of energy transfer to bulk chlorophylls. Biochim Biophys Acta 1557: 91–98 PubMed
Kouřil R, Strouhal O, Nosek L, Lenobel R, Chamrád I, Boekema EJ, Šebela M, Ilík P(2014) Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J 77: 568–576 PubMed
Kubota-Kawai H, Burton-Smith RN, Tokutsu R, Song C, Akimoto S, Yokono M, Ueno Y, Kim E, Watanabe A, Murata K, et al. (2019) Ten antenna proteins are associated with the core in the supramolecular organization of the photosystem I supercomplex in PubMed PMC
Kyle DJ, Staehelin LA, Arntzen CJ(1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222: 527–541 PubMed
Le Quiniou C, Tian L, Drop B, Wientjes E, van Stokkum IHM, van Oort B, Croce R(2015b) PSI-LHCI of PubMed PMC
Le Quiniou C, van Oort B, Drop B, van Stokkum IHM, Croce R(2015a) The high efficiency of photosystem I in the green alga PubMed PMC
Mazor Y, Borovikova A, Caspy I, Nelson N(2017) Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat Plants 3: 17014. PubMed
Metzger P, Largeau C(2005) PubMed
Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M(2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21: 6709–6720 PubMed PMC
Mozzo M, Mantelli M, Passarini F, Caffarri S, Croce R, Bassi R(2010) Functional analysis of Photosystem I light-harvesting complexes (Lhca) gene products of PubMed
Nawrocki WJ, Santabarbara S, Mosebach L, Wollman FA, Rappaport F(2016) State transitions redistribute rather than dissipate energy between the two photosystems in PubMed
Neilson JAD, Durnford DG(2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106: 57–71 PubMed
Oostergetel GT, Keegstra W, Brisson A(1998) Automation of specimen selection and data acquisition for protein electron crystallography. Ultramicroscopy 74: 47–59
Ozawa S-I, Bald T, Onishi T, Xue H, Matsumura T, Kubo R, Takahashi H, Hippler M, Takahashi Y(2018) Configuration of ten light-harvesting chlorophyll PubMed PMC
Pan X, Su X, Cao P, Chang W, Liu Z, Zhang X, Li M(2018) Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II. Science 1113: 1109–1113 PubMed
Pi X, Tian L, Dai H-E, Qin X, Cheng L, Kuang T, Sui S-F, Shen J-R(2018) Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc Natl Acad Sci USA 115: 4423–4428 PubMed PMC
Pietrzykowska M, Suorsa M, Semchonok DA, Tikkanen M, Boekema EJ, Aro E-M, Jansson S(2014) The light-harvesting chlorophyll PubMed PMC
Pinnola A, Alboresi A, Nosek L, Semchonok D, Rameez A, Trotta A, Barozzi F, Kouřil R, Dall’Osto L, Aro E-M, et al. (2018) A LHCB9-dependent photosystem I megacomplex induced under low light in PubMed
Qin X, Pi X, Wang W, Han G, Zhu L, Liu M, Cheng L, Shen JR, Kuang T, Sui SF(2019) Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat Plants 5: 263–272 PubMed
Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC(1999) The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60: 209–215
Romero E, Mozzo M, van Stokkum IHM, Dekker JP, van Grondelle R, Croce R(2009) The origin of the low-energy form of photosystem I light-harvesting complex Lhca4: Mixing of the lowest exciton with a charge-transfer state. Biophys J 96: L35–L37 PubMed PMC
Schägger H.(2006) Tricine—SDS-PAGE. Nat Protoc 1: 16–23 PubMed
Shen L, Huang Z, Chang S, Wang W, Wang J, Kuang T, Han G, Shen JR, Zhang X(2019) Structure of a C PubMed PMC
Snellenburg JJ, Laptenok SP, Seger R, Mullen KM, van Stokkum IHM(2012) Glotaran : A Java-based graphical user interface for the R package TIMP. J Stat Softw 49: 1–22
Su X, Ma J, Pan X, Zhao X, Chang W, Liu Z, Zhang X, Li M(2019) Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex. Nat Plants 5: 273–281 PubMed
Su X, Wei X, Zhu D, Chang W, Liu Z, Zhang X, Li M(2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 820: 815–820 PubMed
Suga M, Ozawa S-I, Yoshida-Motomura K, Akita F, Miyazaki N, Takahashi Y(2019) Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I. Nat Plants 5: 626–636 PubMed
Suga M, Shen JR(2020) Structural variations of photosystem I-antenna supercomplex in response to adaptations to different light environments. Curr Opin Struct Biol 63: 10–17 PubMed
Swingley WD, Iwai M, Chen Y, Ozawa S-I, Takizawa K, Takahashi Y, Minagawa J(2010) Characterization of photosystem I antenna proteins in the prasinophyte PubMed
Tasić MB, Pinto LFR, Klein BC, Veljković VB, Filho RM(2016)
van den Berg TE, Chukhutsina VU, van Amerongen H, Croce R, van Oort B(2019) Light acclimation of the colonial green alga PubMed PMC
van den Berg TE, van Oort B, Croce R(2018) Light-harvesting complexes of PubMed PMC
van Stokkum IHM, Larsen DS, van Grondelle R(2004) Global and target analysis of time-resolved spectra. Biochim Biophys Acta 1657: 82–104 PubMed
Varsano T, Wolf SG, Pick U(2006) A chlorophyll PubMed
Wake L, Hillen L(1980) Study of a “bloom” of the oil‐rich alga
Watanabe M, Semchonok DA, Webber-Birungi MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M(2014) Attachment of phycobilisomes in an antenna-photosystem I supercomplex of cyanobacteria. Proc Natl Acad Sci USA 111: 2512–2517 PubMed PMC
Wientjes E, Oostergetel GT, Jansson S, Boekema EJ, Croce R(2009) The role of Lhca complexes in the supramolecular organization of higher plant photosystem I. J Biol Chem 284: 7803–7810 PubMed PMC
Wientjes E, van Amerongen H, Croce R(2013a) LHCII is an antenna of both photosystems after long-term acclimation. Biochim Biophys Acta 1827: 420–426 PubMed
Wientjes E, van Amerongen H, Croce R(2013b) Quantum yield of charge separation in photosystem II: Functional effect of changes in the antenna size upon light acclimation. J Phys Chem B 117: 11200–11208 PubMed
Wientjes E, van Stokkum IHM, van Amerongen H, Croce R(2011) The role of the individual Lhcas in photosystem I excitation energy trapping. Biophys J 101: 745–754 PubMed PMC
A kaleidoscope of photosynthetic antenna proteins and their emerging roles
Revealing the architecture of the photosynthetic apparatus in the diatom Thalassiosira pseudonana