[en] Phycobilisomes (PBS) are accessory light harvesting protein complexes that directionally transfer energy towards photosystems. Phycobilisomes are organized in a central core and rods radiating from it. Components of phycobilisomes in Gracilaria chilensis (Gch) are Phycobiliproteins (PBPs), Phycoerythrin (PE), and Phycocyanin (PC) in the rods, while Allophycocyanin (APC) is found in the core, and linker proteins (L). The function of such complexes depends on the structure of each component and their interaction. The core of PBS from cyanobacteria is mainly composed by cylinders of trimers of alpha and beta subunits forming heterodimers of Allophycocyanin, and other components of the core including subunits alphaII and beta18. As for the linkers, Linker core (LC) and Linker core membrane (LCM) are essential for the final emission towards photoreaction centers. Since we have previously focused our studies on the rods of the PBS, in the present article we investigated the components of the core in the phycobilisome from the eukaryotic algae, Gracilaria chilensis and their organization into trimers. Transmission electron microscopy provided the information for a three cylinders core, while the three dimensional structure of Allophycocyanin purified from Gch was determined by X-ray diffraction method and the biological unit was determined as a trimer by size exclusion chromatography. The protein sequences of all the components of the core were obtained by sequencing the corresponding genes and their expression confirmed by transcriptomic analysis. These subunits have seldom been reported in red algae, but not in Gracilaria chilensis. The subunits not present in the crystallographic structure were modeled to build the different composition of trimers. This article proposes structural models for the different types of trimers present in the core of phycobilisomes of Gch as a first step towards the final model for energy transfer in this system.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Dagnino-Leone, Jorge
Figueroa, Maximiliano
Mella, Claudia
Vorphal, Maria Alejandra
Kerff, Frédéric ; Université de Liège > Département des sciences de la vie > Centre d'ingénierie des protéines
Vasquez, Aleikar Jose
Bunster, Marta
Martinez-Oyanedel, Jose
Language :
English
Title :
Structural models of the different trimers present in the core of phycobilisomes from Gracilaria chilensis based on crystal structures and sequences.
Publication date :
2017
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Adir N. Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res. 2005; 85: 15-32. https://doi.org/10.1007/s11120-004-2143-y PMID: 15977057
Sun L, Wang S, Zhao M, Fu X, Gong X, Chen M, et al. Phycobilisomes from Cyanobacteria. Handbook on Cyanobacteria: Biochemistry, Biotechnology and Applications. Nova Science Publishers; 2009. pp. 105-160.
Sidler WA. Phycobilisome and Phycobiliprotein Structures. In: Bryant DA, editor. The Molecular Biology of Cyanobacteria. Springer Netherlands; 1994. pp. 139-216.
MacColl R. Allophycocyanin and energy transfer. Biochim Biophys Acta BBA - Bioenerg. 2004; 1657: 73-81.
Arteni AA, Ajlani G, Boekema EJ. Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim Biophys Acta BBA - Bioenerg. 2009; 1787: 272-279.
Hagopian JC, Reis M, Kitajima JP, Bhattacharya D, Oliveira MC de. Comparative Analysis of the Complete Plastid Genome Sequence of the Red Alga Gracilaria tenuistipitata var. liui Provides Insights into the Evolution of Rhodoplasts and Their Relationship to Other Plastids. J Mol Evol. 2004; 59: 464-477. https://doi.org/10.1007/s00239-004-2638-3 PMID: 15638458
Lundell DJ, Glazer AN. Molecular architecture of a light-harvesting antenna. Core substructure in Synechococcus 6301 phycobilisomes: two new allophycocyanin and allophycocyanin B complexes. J Biol Chem. 1983; 258: 902-908. PMID: 6401721
Maxson P, Sauer K, Zhou J, Bryant DA, Glazer AN. Spectroscopic studies of cyanobacterial phycobilisomes lacking core polypeptides. Biochim Biophys Acta BBA - Bioenerg. 1989; 977: 40-51.
Houmard J, Capuano V, Colombano MV, Coursin T, Marsac NT de. Molecular characterization of the terminal energy acceptor of cyanobacterial phycobilisomes. Proc Natl Acad Sci. 1990; 87: 2152-2156. PMID: 2107546
Gao X, Wei T-D, Zhang N, Xie B-B, Su H-N, Zhang X-Y, et al. Molecular insights into the terminal energy acceptor in cyanobacterial phycobilisome. Mol Microbiol. 2012; 85: 907-915. https://doi.org/10.1111/j.1365-2958.2012.08152.x PMID: 22758351
Mullineaux CW. Phycobilisome-reaction centre interaction in cyanobacteria. Photosynth Res. 2008; 95: 175. https://doi.org/10.1007/s11120-007-9249-y PMID: 17922214
Reuter W, Wiegand G, Huber R, Than ME. Structural analysis at 2.2 Å of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP LC7. 8, from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci. 1999; 96: 1363-1368. PMID: 9990029
Zhao K-H, Su P, Böhm S, Song B, Zhou M, Bubenzer C, et al. Reconstitution of phycobilisome core-membrane linker, LCM, by autocatalytic chromophore binding to ApcE. Biochim Biophys Acta BBA - Bioenerg. 2005; 1706: 81-87.
Adir N, Dines M, Klartag M, McGregor A, Melamed-Frank M. Assembly and Disassembly of Phycobilisomes. In: Shively JM, editor. Complex Intracellular Structures in Prokaryotes. Springer Berlin Heidelberg; 2006. pp. 47-77.
Jallet D, Gwizdala M, Kirilovsky D. ApcD, ApcF and ApcE are not required for the Orange Carotenoid Protein related phycobilisome fluorescence quenching in the cyanobacterium Synechocystis PCC 6803. Biochim Biophys Acta BBA - Bioenerg. 2012; 1817: 1418-1427.
Capuano V, Braux AS, Marsac NT de, Houmard J. The "anchor polypeptide" of cyanobacterial phycobilisomes. Molecular characterization of the Synechococcus sp. PCC 6301 apce gene. J Biol Chem. 1991; 266: 7239-7247. PMID: 1901865
Watanabe M, Ikeuchi M. Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res. 2013; 116: 265-276. https://doi.org/10.1007/s11120-013-9905-3 PMID: 24081814
Bird CJ, McLachlan J, Oliveira EC de. Gracilaria chilensis sp.nov. (Rhodophyta, Gigartinales), from Pacific South America. Can J Bot. 1986; 64: 2928-2934.
Contreras-Martel C, Matamala A, Bruna C, Poo-Caamaño G, Almonacid D, Figueroa M, et al. The structure at 2 Å resolution of Phycocyanin from Gracilaria chilensis and the energy transfer network in a PC-PC complex. Biophys Chem. 2007; 125: 388-396. https://doi.org/10.1016/j.bpc.2006.09.014 PMID: 17118524
Contreras-Martel C, Martinez-Oyanedel J, Bunster M, Legrand P, Piras C, Vernede X, et al. Crystallization and 2.2 Å resolution structure of R-phycoerythrin from Gracilaria chilensis: a case of perfect hemihedral twinning. Acta Crystallogr D Biol Crystallogr. 2001; 57: 52-60. PMID: 11134927
Figueroa M, Martínez-Oyanedel J, Matamala AR, Dagnino-Leone J, Mella C, Fritz R, et al. In silico model of an antenna of a phycobilisome and energy transfer rates determination by theoretical Förster approach. Protein Sci. 2012; 21: 1921-1928. https://doi.org/10.1002/pro.2176 PMID: 23047609
Collén J, Porcel B, Carré W, Ball SG, Chaparro C, Tonon T, et al. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci. 2013; 110: 5247-5252. https://doi.org/10.1073/pnas.1221259110 PMID: 23503846
Guan X, Qin S, Zhao F, Zhang X, Tang X, others. Phycobilisomes linker family in cyanobacterial genomes: divergence and evolution. Int J Biol Sci. 2007; 3: 434-445. PMID: 18026567
Vorphal MA, Gallardo-Escárate C, Valenzuela-Muñoz V, Dagnino-Leone J, Vásquez JA, Martínez-Oyanedel J, et al. De novo transcriptome analysis of the red seaweed Gracilaria chilensis and identification of linkers associated with phycobilisomes. Mar Genomics. 2017; 31: 17-19. https://doi.org/10.1016/j.margen.2016.11.001 PMID: 27843115
Liu J-Y, Jiang T, Zhang J-P, Liang D-C. Crystal Structure of Allophycocyanin from Red AlgaePorphyra yezoensis at 2.2-Å Resolution. J Biol Chem. 1999; 274: 16945-16952. PMID: 10358042
Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010; 66: 213-221. https://doi.org/10.1107/S0907444909052925 PMID: 20124702
Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004; 60: 2126-2132. https://doi.org/10.1107/S0907444904019158 PMID: 15572765
Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr. 2012; 68: 352-367. https://doi.org/10.1107/S0907444912001308 PMID: 22505256
Webb B, Sali A. Comparative Protein Structure Modeling Using MODELLER. Current Protocols in Bioinformatics. John Wiley & Sons, Inc.; 2002.
Tang K, Ding W-L, Höppner A, Zhao C, Zhang L, Hontani Y, et al. The terminal phycobilisome emitter, LCM: A light-harvesting pigment with a phytochrome chromophore. Proc Natl Acad Sci. 2015; 112: 15880-15885. https://doi.org/10.1073/pnas.1519177113 PMID: 26669441
Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007; 35: W407-W410. https://doi.org/10.1093/nar/gkm290 PMID: 17517781
Lovell SC, Davis IW, Arendall WB, de Bakker PIW, Word JM, Prisant MG, et al. Structure validation by Cα geometry: φ,ψ and Cβ deviation. Proteins Struct Funct Bioinforma. 2003; 50: 437-450.
Tu P, Yao Y, Li Y, Liu B. Conformational flexibility of phycocyanobilin: Monte-Carlo and DFT study. J Mol Struct THEOCHEM. 2009; 894: 9-13.
Göller AH, Strehlow D, Hermann G. Conformational Flexibility of Phycocyanobilin: An AM1 Semiempirical Study. ChemPhysChem. 2001; 2: 665-671. https://doi.org/10.1002/1439-7641(20011119)2:11〈665::AID-CPHC665〉3.0.CO;2-O PMID: 23686901
Piovesan D, Tabaro F, Mičetić I, Necci M, Quaglia F, Oldfield CJ, et al. DisProt 7.0: a major update of the database of disordered proteins. Nucleic Acids Res. 2017; 45: D1123-D1124. https://doi.org/10.1093/nar/gkw1279 PMID: 27965415
Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D, Adir N. Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci. 2016; 113: E1655-E1662. https://doi.org/10.1073/pnas.1523680113 PMID: 26957606
Tal O, Trabelcy B, Gerchman Y, Adir N. Investigation of Phycobilisome Subunit Interaction Interfaces by Coupled Cross-linking and Mass Spectrometry. J Biol Chem. 2014; jbc.M114.595942.
Kuzminov FI, Bolychevtseva YV, Elanskaya IV, Karapetyan NV. Effect of APCD and APCF subunits depletion on phycobilisome fluorescence of the cyanobacterium Synechocystis PCC 6803. J Photochem Photobiol B. 2014; 133: 153-160. https://doi.org/10.1016/j.jphotobiol.2014.03.012 PMID: 24727864
Chang L, Liu X, Li Y, Liu C-C, Yang F, Zhao J, et al. Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res. 2015; 25: 726-737. https://doi.org/10.1038/cr.2015.59 PMID: 25998682