Skip to main content
Log in

Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Phycobilisome (PBS) is a giant water-soluble photosynthetic antenna transferring the energy of absorbed light mainly to the photosystem II (PSII) in cyanobacteria. Under the low light conditions, PBSs and PSII dimers form coupled rows where each PBS is attached to the cytoplasmic surface of PSII dimer, and PBSs come into contact with their face surfaces (state 1). The model structure of the PBS core that we have developed earlier by comparison and combination of different fine allophycocyanin crystals, as reported in Zlenko et al. (Photosynth Res 130(1):347–356, 2016b), provides a natural way of the PBS core face-to-face stacking. According to our model, the structure of the protein–protein contact between the neighboring PBS cores in the rows is the same as the contact between the APC hexamers inside the PBS core. As a result, the rates of energy transfer between the cores can occur, and the row of PBS cores acts as an integral PBS “supercore” providing energy transfer between the individual PBS cores. The PBS cores row pitch in our elaborated model (12.4 nm) is very close to the PSII dimers row pitch obtained by the electron microscopy (12.2 nm) that allowed to unite a model of the PBS cores row with a model of the PSII dimers row. Analyzing the resulting model, we have determined the most probable locations of ApcD and ApcE terminal emitter subunits inside the bottom PBS core cylinders and also revealed the chlorophyll molecules of PSII gathering energy from the PBS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85:15–32

    Article  CAS  PubMed  Google Scholar 

  • Anderson LK, Eiserling FA (1986) Asymmetrical core structure in phycobilisomes of the cyanobacterium Synechocystis  \(6701\). J Mol Biol 191(3):441–451

    Article  CAS  PubMed  Google Scholar 

  • Arteni AA, Liu LN, Aartsma TJ, Zhang YZ, Zhoua BC, Boekema EJ (2008) Structure and organization of phycobilisomes on membranes of the red alga Porphyridium cruentum. Photosynth Res 95(2–3):169–174

    Article  CAS  PubMed  Google Scholar 

  • Arteni AA, Ajlani G, Boekema EJ (2009) Structural organization of phycobilisomes from Synechocystis strain PCC \(6803\) and their interaction with the membrane. Biochim Biophys Acta 1787(4):272–279

    Article  CAS  PubMed  Google Scholar 

  • Ashby MK, Mullineaux CW (1999) The role of ApcD and ApcF in energy transfer from phycobilisomes to PS I and PS II in a cyanobacterium. Photosynth Res 61:169–179

    Article  CAS  Google Scholar 

  • Bald D, Kruip J, Rögner M (1996) Supramolecular architecture of cyanobacterial thylakoid membranes: how is the phycobilisome connected with the photosystems? Photosynth Res 49:103–118

    Article  CAS  PubMed  Google Scholar 

  • Barber J, Morris EP, da Fonseca PC (2003) Interaction of the allophycocyanin core complex with photosystem II. Photochem Photobiol Sci 2(5):536–541

    Article  CAS  PubMed  Google Scholar 

  • Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189(3):366–383

    Article  CAS  PubMed  Google Scholar 

  • Brejc K, Ficner R, Huber R, Steinbacher S (1995) Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at \(2.3\) Å resolution. J Mol Biol 249(2):424–440

    Article  CAS  PubMed  Google Scholar 

  • Bryant DA (1991) Cyanobacterial phycobilisomes: progress towards complete structural and functional analysis via molecular genetics. In: Bogorad L, Vasil I (eds) Cell culture and somatic cell genetics of plants. Academic Press, San Diego, pp 257–300

    Google Scholar 

  • Bryant DA, Guglielmi G, de Marsac NT, Castets AM, Cohen-Bazire G (1979) The structure of cyanobacterial phycobilisomes: a model. Arch Microbiol 123(2):113–127

    Article  CAS  Google Scholar 

  • Capuano V, Braux AS, de Marsac NT, Houmard J (1991) The “anchor polypeptide” of cyanobacterial phycobilisomes. Molecular characterisation of the Synechococcus sp. PCC 6301 apce gene. J Biol Chem 266(11):7239–7247

    CAS  PubMed  Google Scholar 

  • Capuano V, Thomas JC, de Marsac NT, Houmard J (1993) An in vivo approach to define the role of the \({\text L}_{\text CM}\), the key polypeptide of cyanobacterial phycobilisomes. J Biol Chem 268(11):8277–8283

    CAS  PubMed  Google Scholar 

  • Chang L, Liu X, Li Y, Liu C, Yang F, Zhao J, Sui S (2015) Structural organization of an intact phycobilisome and its association with photosystem II. Cell Res 25:726–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David L, Prado M, Arteni AA, Elmlund DA, Blankenship RE, Adir N (2014) Structural studies show energy transfer within stabilized phycobilisomes independent of the mode of rod-core assembly. Biochim Biophys Acta 1837(3):385–395

    Article  CAS  PubMed  Google Scholar 

  • Dekker J, Boekema EJ, Witt H, Rögner M (1988) Refined purification and further characterization of oxygen-evolving and tris-treated photosystem II particles from the thermophilic cyanobacterium Synechococcus sp. Biochim Biophys Acta 936:307–318

    Article  CAS  Google Scholar 

  • Delphin E, Duval JC, Kirilovsky D (1995) Comparison of state 1 - state 2 transitions in the green alga Chlamydomonas reinhardtii and in the red alga Rhodella violacea: effect of kinase and phosphatase inhibitors. Biochim Biophys Acta 1232:91–95

    Article  Google Scholar 

  • Dong C, Tang A, Zhao J, Mullineaux CW, Shen G, Bryant DA (2009) ApcD is necessary for efficient energy transfer from phycobilisomes to photosystem I and helps to prevent photoinhibition in the cyanobacterium Synechococcus sp. PCC \(7002\). Biochim Biophys Acta 1787:1122–1128

    Article  CAS  PubMed  Google Scholar 

  • Ducret A, Müller SA, Goldie KN, Hefti A, Sidler WA, Zuber H, Engel A (1998) Reconstitution, characterisation and mass analysis of the pentacylindrical allophycocyanin core complex from the cyanobacterium Anabaena sp. PCC \(7120\). J Mol Biol 278:369–388

    Article  CAS  PubMed  Google Scholar 

  • Emlyn-Jones D, Ashby MK, Mullineaux CW (1999) A gene required for the regulation of photosynthetic light harvesting in the cyanobacterium Synechocystys  \(6803\). Mol Microbiol 33(5):1050–1058

    Article  CAS  PubMed  Google Scholar 

  • Folea IM, Zhang P, Arob EM, Boekema EJ (2008) Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC \(6803\) investigated by electron microscopy. FEBS Lett 582(12):1749–1754

    Article  CAS  PubMed  Google Scholar 

  • Fork DC, Mohanty P (2012) Fluorescence and other characteristics of blue-green algae (cyanobacteria), red algae, and cryptomonads. In: Amesz J (ed) Light emission by plants and bacteria, chap 16. Elsevier, Amsterdam, pp 451–496

  • Förster T (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann der Physik 437(1–2):55–75

    Article  Google Scholar 

  • Füglistaller P, Mimuro M, Suter F, Zuber H (1987) Allophycocyanin complexes of the phycobilisome from Mastigocladus laminosus. Hoppe-Seyler’s Z Physiol Chem 368:353–367

    Google Scholar 

  • Gao X, Zhang N, Wei TD, Su HN, Xie BB, Dong CC, Zhang XY, Chen XL, Zhou BC, Wang ZX, Wu JW, Zhang YZ (2011) Crystal structure of the N-terminal domain of linker L\(_{\rm R}\) and the assembly of cyanobacterial phycobilisome rods. Mol Microbiol 82(3):698–705

    Article  CAS  PubMed  Google Scholar 

  • Giddings TH, Wasmann C, Staehelin LA (1983) Structure of the thylakoids and envelope membranes of the cyanelles of Cyanophora paradoxa. Plant Physiol 71:409–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gindt YM, Zhou J, Bryant D, Sauer K (1992) Core mutations of Synechococcus sp. PCC 7002 phycobilisomes: a spectroscopic study. J Photochem Photobiol B 15(3):75–89

    Article  CAS  PubMed  Google Scholar 

  • Gindt YM, Zhou J, Bryant D, Sauer K (1994) Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: assignment of excited state energies to the \(L_{CM}\), \(\beta ^{18}\) and \(\alpha ^{\beta }\) chromophores. Biochim Biophys Acta 1186(3):153–162

    Article  CAS  PubMed  Google Scholar 

  • Gingrich JC, Lundell DJ, Glazer AN (1983) Core substructure in cyanobacterial phycobilisomes. J Cell Biochem 22(1):1–14

    Article  CAS  PubMed  Google Scholar 

  • Glauser M, Bryant DA, Frank G, Wehrli E, Rusconi SS, Sidler W, Zuber H (1992) Phycobilisome structure in the cyanobacteria Mastigocladus laminosus and Anabaena sp. PCC \(7120\). Eur J Biochem 205:907–915

    Article  CAS  PubMed  Google Scholar 

  • Guglielmi G, Cohen-Bazire G, Bryant DA (1981) The structure of Gloeobacter violaceus and its phycobilisomes. Arch Microbiol 129:181–189

    Article  CAS  Google Scholar 

  • Harris D, Tal O, Jallet D, Wilson A, Kirilovsky D, Adir N (2016) Orange carotenoid protein burrows into the phycobilisome to provide photoprotection. Proc Natl Acad Sci USA 113(13):E1655–E1662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellmich J, Bommer M, Burkhardt A, Ibrahim M, Kern J, Meents A, Holger D, Muh F, Zouni A (2014) Native-like photosystem II superstructure at \(2.44\) Å resolution through detergent extraction from the protein crystal. Structure 22(11):1607–1615

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Marquardt J, Iwasaki I, Miyashita H, Kurano N, Mörschel E, Miyachi S (1999) Molecular structure, localization and function of biliproteins in the chlorophyll a/d containing oxygenic photosynthetic prokaryote Acaryochloris marina. Biochim Biophys Acta 1412(3):250–261

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA (2004) Structure and function of the water-soluble carotenoid-binding proteins of cyanobacteria. Photosynth Res 81(3):215–225

    Article  CAS  PubMed  Google Scholar 

  • Khanna R, Graham JR, Myers J, Gantt E (1983) Phycobilisome composition and possible relationship to reaction centers. Arch Biochem Biophys 224(2):534–542

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D (2015) Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions. Photosynth Res 126:3–17

    Article  CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2016) Cyanobacterial photoprotection by the orange carotenoid protein. Nat Plants 2(16):180

    Google Scholar 

  • Kirilovsky D, Kana R, Prasil O (2014) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht

    Google Scholar 

  • Koyama K, Tsuchiya T, Akimoto S, Yokono M, Miyashita H, Mimuro M (2006) New linker proteins in phycobilisomes isolated from the cyanobacterium Gloeobacter violaceus PCC 7421. FEBS lett 580:3457–3461

    Article  CAS  PubMed  Google Scholar 

  • Kruip J, Chitnis P, Lagoutte B, Roegner M, Boekema E (1997) Structural organization of the major subunits in cyanobacterial photosystem I. Localization of subunits PsaC, -D, -E, -F, and -J. J Biol Chem 272:17061–17069

    Article  CAS  PubMed  Google Scholar 

  • Kuhl H, Rögner M, van Breemen JF, Boekema EJ (1999) Localization of cyanobacterial photosystem II donor-side subunits by electron microscopy and the supramolecular organization of photosystem II in the thylakoid membrane. Eur J Biochem 266:453–459

    Article  CAS  PubMed  Google Scholar 

  • Kuzminov F, Bolychevtseva Y, Karapetyan NV, Elanskaya IV (2014) Effect of ApcD and ApcF subunits depletion on phycobilisome fluorescence of the cyanobacterium Synechocystis PCC \(6803\). J Photochem Photobiol B 133:153–160

    Article  CAS  PubMed  Google Scholar 

  • Lefort-Tran M, Cohen-Bazire G, Pouphile M (1973) Les membranes photosynthétiques des algues á biliproteines observées apres cryodécapage. J Ultrastruct Res 44:199–209

    Article  CAS  PubMed  Google Scholar 

  • Leverenz RL, Jallet D, Li MD, Mathies RA, Kirilovsky D, Kerfeld CA (2014) Structural and functional modularity of the orange carotenoid protein: Distinct roles for the N- and C-terminal domains in cyanobacterial photoprotection. Plant Cell 26(1):426–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leverenz RL, Sutter M, Wilson A, Gupta S, Thurotte A, de Carbon CB, Petzold CJ, Ralston C, Perreau F, Kirilovsky D, Kerfeld CA (2015) A \(12\) Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348(6242):1463–1466

    Article  CAS  PubMed  Google Scholar 

  • Lichté C, Thomas J (1976) Étude ultrastructurale des thylacoïdes des algues á phycobiliproteines, comparaison des résultats obtenus par fixation classique et cryodécapage. Phycologia 15:393–404

    Article  Google Scholar 

  • Liu H, Zhang H, Niedzwiedzki DM, Prado M, He G, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342(6162):1104–1107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Zhang H, Orf GS, Lu Y, Jiang J, King JD, Wolf NR, Gross ML, Blankenship RE (2016) Dramatic domain rearrangements of the cyanobacterial orange carotenoid protein upon photoactivation. Biochemistry 55(7):1003–1009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JY, Jiang T, Zhang JP, Liang DC (1999) Crystal structure of allophycocyanin from red algae Porphyra yezoensis at \(2.2\) Å resolution. J Biol Chem 274(24):16945–16952

    Article  CAS  PubMed  Google Scholar 

  • Liu LN, Chen XL, Zhang YZ, Zhou BC (2005) Characterization, structure and function of linker polypeptides in phycobilisomes of cyanobacterria and red algae. Biochim Biophys Acta 1708(2):133–142

    Article  CAS  PubMed  Google Scholar 

  • Lundell DJ, Glazer AN (1981) Allophycocyanin B. J Biol Chem 256(23):12600–12606

    CAS  PubMed  Google Scholar 

  • Lundell DJ, Glazer AN (1983) Molecular architecture of a light-harvesting antenna. Core substructure in Synechococcus 6301 phycobilisomes: Two new allophycocyanin and allophycocyanin B complexes. J Biol Chem 258(2):902–908

    CAS  PubMed  Google Scholar 

  • Lundell DJ, Glazer AN (1983) Molecular architecture of a light-harvesting antenna. FCore substructure in Synechococcus 6301 phycobilisomes: Quaternary interaction in the Synechococcus  \(6301\) phycobilisome core as revealed by partial tryptic digestion and circular dichroism studies. J Biol Chem 258(14):8708–8713

    CAS  PubMed  Google Scholar 

  • Lundell DJ, Glazer AN (1983) Molecular architecture of a light-harvesting antenna. Structure of the 18S core-rod subassembly of the Synechococcus 6301 phycobilisome. J Biol Chem 258(2):894–901

    CAS  PubMed  Google Scholar 

  • Macindoe G, Mavridis L, Venkatraman V, Devignes MD, Ritchie DW (2010) Hexserver: an FFT-based protein docking server powered by graphics processors. Nucl Acid Res 38:W445–W449

    Article  CAS  Google Scholar 

  • Maksimov EG, Moldenhauer M, Shirshin EA, Parshina EA, Sluchanko N, Klementiev KE, Tsoraev GV, Willoweit NTM, Schmitt FJ, Sandmann JBG, Paschenko VZ, Friedrich T, Rubin AB (2016) A comparative study of three signaling forms of the orange carotenoid protein. Photosynth Res 130(1):389–401

    Article  CAS  PubMed  Google Scholar 

  • Marquardt J, Senger H, Miyashita H, Miyachi S, Mörschel E (1997) Isolation and characterization of biliprotein aggregates from Acaryochloris marina, a Prochloron-like prokaryote containing mainly chlorophyll d. FEBS Lett 410:428–432

    Article  CAS  PubMed  Google Scholar 

  • Marx A, Adir N (2013) Allophycocyanin and phycocyanin crystal structures reveal facets of phycobilisome assembly. Biochim Biophys Acta 1827:311–318

    Article  CAS  PubMed  Google Scholar 

  • McGregor A, Klartag M, David L, Adir N (2008) Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. J Mol Biol 384:406–421

    Article  CAS  PubMed  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058(2):87–106

    Article  CAS  Google Scholar 

  • Mimuro M, Fujita Y (1978) Excitation energy transfer between pigment system II units in blue-green algae. Biochim Biophys Acta 504:406–412

    Article  CAS  PubMed  Google Scholar 

  • Mimuro M, Lipschultz C, Gantt E (1986) Energy flow in the phycobilisome core of Nostoc sp. (MAC): two independent terminal pigments. Biochim Biophys Acta 852(1):126–132

    Article  CAS  Google Scholar 

  • Mimuro M, Kikuchi H, Murakami A (1999) Structure and function of phycobilisomes. In: Singhal G, Renger G, Sopory S, Irrgang K, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis, chap 5. Narosa Publishing House, New Delhi, pp 104–135

  • Mörschel E, Mühlethaler K (1983) On the linkage of exoplasmatic freeze-fracture particles to phycobilisomes. Planta 158(5):451–457

    Article  PubMed  Google Scholar 

  • Mörschel E, Schatz GH (1987) Correlation of photosystem-II complexes with exoplasmatic freeze-fracture particles of thylakoids of the cyanobacterium Synechococcus sp. Planta 172(2):145–154

    Article  PubMed  Google Scholar 

  • Mörschel E, Koller KP, Wehrmeyer W, Schneider H (1977) Biliprotein assembly in the disc-shaped phycobilisomes of Rhodella violacea. I. Electron microscopy of phycobilisomes in situ and analysis of their architecture after isolation and negative staining. Cytobiologie 16:118–129

    Google Scholar 

  • Mullineaux CW (1994) Excitation energy transfer from phycobilisomes to photosystem I in cyanobacterial mutant lacking photosystem II. Biochim Biophys Acta 1184(1):71–77

    Article  CAS  Google Scholar 

  • Mullineaux CW, Allen JF (1988) Fluorescence induction transients indicate dissociation of photosystem II from the phycobilisome during the state-\(2\) transition in the cyanobacterium Synechococcus  \(6301\). Biochim Biophys Acta 934(1):96–107

    Article  CAS  Google Scholar 

  • Mullineaux CW, Allen JF (1990) State \(1\) - state \(2\) transitions in the cyanobacterium Synechococcus  \(6301\) are controlled by the redox state of electron carriers between photosystems I and II. Photosynth Res 23(3):297–311

    Article  CAS  PubMed  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172(2):242–251

    Article  CAS  PubMed  Google Scholar 

  • Murray J, Maghlaoui K, Barber J (2007) The structure of allophycocyanin from Thermosynechococcus elongatus at \(3.5\) Å resolution. Acta Cryst F63:998–1002

    Google Scholar 

  • Nganou C, David L, Adir N, Mkandawire M (2016) Linker proteins enable ultrafast excitation energy transfer in the phycobilisome antenna system of Thermosynechococcus vulcanus. Photochem Photobiol Sci 15(1):31–44

    Article  CAS  PubMed  Google Scholar 

  • Nilsson F, Simpson DJ, Jansson C, Andersson B (1992) Ultrastructural and biochemical characterization of a Synechocystis  \(6803\) mutant with inactivated psbA genes. Arch Biochem Biophys 292(2):340–347

    Article  Google Scholar 

  • Olive J, M’Bina I, Vernotte C, Astier C, Wollman F (1986) Randomization of the EF particles in thylakoid membranes of Synechocystis  \(6714\) upon transition from state I to state II. FEBS Lett 208(2):203–212

    Article  Google Scholar 

  • Olive J, Ajlani G, Astier C, Recouvreur M, Vernotte C (1997) Ultrastructure and light adaptation of phycobilisome mutants of Synechocystis PCC \(6803\). Biochim Biophys Acta 1319(2):275–282

    Article  CAS  Google Scholar 

  • Peng PP, Dong LL, Sun YF, Zeng XL, Ding WL, Scheer H, Yang X, Zhao KH (2014) The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme red shift of the terminal emitter in phycobilisomes. Acta Cryst D70:2558–2569

    Google Scholar 

  • Rakhimberdieva MG, Boichenko VA, Karapetyan NV, Stadnichuk IN (2001) Interaction of phycobilisomes with photosystem II dimers and photosystem I monomers and trimers in the cyanobacterium Spirulina platensis. Biochemistry 40(51):15780–15788

    Article  CAS  PubMed  Google Scholar 

  • Rakhimberdieva MG, Stadnichuk IN, Elanskaya IV, Karapetyan NV (2004) Carotenoid-induced quenching of the phycobilisome fluorescence in photosystem II-deficient mutant of Synechocystis sp. PCC \(6803\). FEBS Lett 574(1–3):85–88

    Article  CAS  PubMed  Google Scholar 

  • Reuter W, Nickel C, Wehrmeyer W (1990) Isolation of allophycocyanin B from Rhodella violacea results in a model of the core from hemidiscoidal phycobilisomes of rhodophyceae. FEBS Lett 273(1):155–158

    Article  CAS  PubMed  Google Scholar 

  • Reuter W, Wiegand G, Huber R, Than M (1999) Structural analysis at \(2.2\) Å of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, \({\rm AP} \cdot L_C^{7.8}\) from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci USA 96:1363–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosinski J, Hainfeld J, Rigbi M, Siegelman H (1981) Phycobilisome ultrastructure and chromatic adaptation in Fremyella diplosiphon. Ann Bot 47(1):1–12

    Article  Google Scholar 

  • Sidler WA (1994) Phycobilisome and phycobiliprotein structures. In: Bryant DA (ed) The molecular biology of cyanobacteria, chap 7. Springer, Dordrecht, pp 139–216

  • Sonani R, Gupta G, Madamwar D, Kumar V (2015) Crystal structure of allophycocyanin from marine cyanobacterium Phormidium sp. A09DM. PLoS ONE 10(4):e0124580

    Google Scholar 

  • Stadnichuk IN, Bulychev AA, Lukashev EP, Sinetova MP, Khristin MS, Jonson MP, Ruban AV (2011) Far-red light-regulated efficient energy transfer from phycobilisomes to photosystem I in the red microalga Galdieria sulphuraria and photosystem-related heterogeneity of phycobilisome population. Biochim Biophys Acta 1807(2):227–235

    Article  CAS  PubMed  Google Scholar 

  • Stadnichuk IN, Yanyushin MF, Maksimov EG, Lukashev EP, Zharmukhamedov SK, Elanskaya IV, Paschenko VZ (2012) Site of non-photochemical quenching of the phycobilisome by orange carotenoid protein in the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1817(8):1436–1445

    Article  CAS  PubMed  Google Scholar 

  • Stadnichuk IN, Yanyushin MF, Bernát G, Zlenko DV, Krasilnikov PM, Lukashev EP, Maksimov EG, Paschenko VZ (2013) Fluorescence quenching of the phycobilisome terminal emitter L\(_{\rm CM}\) from the cyanobacterium Synechocystis sp. PCC \(6803\) detected in vivo and in vitro. Photochem Photobiol B 125:137–145

    Article  CAS  Google Scholar 

  • Stadnichuk IN, Krasilnikov PM, Zlenko DV, Freidzon AY, Yanyushin MF, Rubin AB (2015) Electronic coupling of the phycobilisome with the orange carotenoid protein and fluorescence quenching. Photosynth Res 124:315–335

    Article  CAS  PubMed  Google Scholar 

  • Tal O, Trabelcy B, Gerchman Y, Adir N (2014) Investigation of phycobilisome subunit interaction interfaces by coupled cross-linking and mass spectrometry. J Biol Chem 289(48):33084–33097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang K, Ding WL, Höppner A, Zhao C, Zhang L, Hontani Y, Kennis JT, Gärtner W, Scheer H, Zhou M, Zhao KH (2015) The terminal phycobilisome emitter, \({\text L}_{\text {CM}}\): a light-harvesting pigment with a phytochrome chromophore. Proc Nat Acad Sci USA 112(52):15880–15885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang RT, Stevens C, Myers J (1977) Action spectra for photoreactions I and II of photosynthesis in the blue-green alga Anacystis nidulans. Photochem Photobiol 25(1):103–108

    Article  CAS  Google Scholar 

  • Watanabe M, Ikeuchi M (2013) Phycobilisome: architecture of a light-harvesting supercomplex. Photosynth Res 116(2):265–276

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Semchonok DA, Webber-Birungic MT, Ehira S, Kondo K, Narikawa R, Ohmori M, Boekema EJ, Ikeuchi M (2014) Attachment of phycobilisomes in an antenna-photosystem I super-complex of cyanobacteria. Proc Nat Acad Sci USA 111(7):2512–2517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westermann M, Wehrmeyer W (1995) A new type of complementary chromatic adaptation exemplified by Phormidium sp. C\(86\): Changes in the number of peripheral rods and in the stoichiometry of core complexes in phycobilisomes. Arch Microbiol 164:132–141

    Article  CAS  Google Scholar 

  • Wildman R, Bowen C (1974) Phycobilisomes in blue-green algae. J Bacteriol 117:866–881

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams RC, Gindrich JC, Glazzer AN (1980) Cyanobacterial phycobilisomes. J Cell Biol 85:558–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanaka G, Glazer AN, Williams RC (1980) Molecular architecture of a light-harvesting antenna. Comparison of wild type and mutant Synechococcus \(6301\) phycobilisomes. J Biol Chem 255(22):11004–11010

    CAS  Google Scholar 

  • Yamanaka G, Lundell DJ, Glazer AN (1982) Molecular architecture of a light-harvesting antenna. Isolation and characterization of phycobilisome subassembly particles. J Biol Chem 257(8):4077–4086

    CAS  PubMed  Google Scholar 

  • Yi ZW, Huang H, Kuang TY, Sui SF (2005) Three-dimensional architecture of phycobilisomes from Nostoc flagelliforme revealed by single particle electron microscopy. FEBS Lett 579:3569–3573

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2014) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochem 53:13–19

    Article  CAS  Google Scholar 

  • Zhang H, Liu H, Lu Y, Wolf NR, Gross ML, Blankenship RE (2016) Native mass spectrometry and ion mobility characterize the orange carotenoid protein functional domains. Biochim Biophys Acta 1857(6):734–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhou J, Bryant DA (1992) Energy transfer processes in phycobilisomes as deduced from analyses of mutants of Synechococcus sp. PCC \(7002\). In: Murata N (ed) Research in photosynthesis, vol 1. Kluwer, Dordrecht, pp 25–32

    Google Scholar 

  • Zlenko DV, Krasilnikov PM, Stadnichuk IN (2016) Role of inter-domain cavity in the attachment of the orange carotenoid protein to the phycobilisome core and to the fluorescence recovery protein. J Biomol Struct Dyn 34(3):486–496

    Article  CAS  PubMed  Google Scholar 

  • Zlenko DV, Krasilnikov PM, Stadnichuk IN (2016) Structural modeling of the phycobilisome core and its association with the photosystems. Photosynth Res 130(1):347–356

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by Russian Science Foundation, Project Number 14-14-00589.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dmitry V. Zlenko.

Additional information

This study is dedicated to Professor G. Riznichenko on the occasion of her 70th birthday.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zlenko, D.V., Galochkina, T.V., Krasilnikov, P.M. et al. Coupled rows of PBS cores and PSII dimers in cyanobacteria: symmetry and structure. Photosynth Res 133, 245–260 (2017). https://doi.org/10.1007/s11120-017-0362-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-017-0362-2

Keywords

Navigation