Skip to main content
SpringerLink
Log in
Book cover

Photosynthesis in Algae: Biochemical and Physiological Mechanisms pp 367–396Cite as

Modulating Energy Transfer from Phycobilisomes to Photosystems: State Transitions and OCP-Related Non-Photochemical Quenching

  • Chapter
  • First Online:

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 45))

Abstract

It is crucial for living organisms to be able to constantly sense and adapt to environmental changes. Light becomes dangerous for photosynthetic organisms when the energy arriving to the photochemical reaction centers exceeds the energy consumption by multiple cellular processes. This occurs under high irradiance but also under nutrient starvation conditions. In these cases, the entire photosynthetic electron transport chain becomes reduced and reactive oxygen species (ROS) leading to severe damage to the cells. Higher plants, eukaryotic algae and cyanobacteria have developed photoprotective mechanisms that decrease the energy arriving at the photochemical reaction centers or balance the energy arriving at each photosystem by regulating the antenna-reaction center interactions. The mechanisms differ in cyanobacteria from those existing in higher plants and eukaryotic algae due to the special cyanobacterial antenna, the phycobilisome (as distinct from the phycobilsome of red algae). In this chapter, two phycobilisome photoprotective mechanisms will be described: the Orange Carotenoid Protein (OCP)-related Non-Photochemical-Quenching (NPQ) and state transitions. The OCP is a photoactive protein that senses light intensity and induces thermal dissipation of excess excitation energy by interacting with the phycobilisome. The OCP-related NPQ is induced only under high irradiance independently of the redox state of the electron transport chain. In contrast, the redox state of the plastoquinone pool regulates state transitions by inducing a restructure of the photosynthetic apparatus. This leads to redistribution of the energy absorbed by the phycobilisomes between the photosystems and/or to changes in excitation energy spillover between photosystems.

*Author for correspondence, e-mail: diana.kirilovsky@cea.fr

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

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

    CAS  PubMed  Google Scholar 

  • Adir N (2008) Structure of the phycobilisome antennae in cyanobacteria and red algae. In: Fromme P (ed) Photosynthetic protein complexes: a structural approach. WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim, pp 243–274

    Google Scholar 

  • Ajlani G, Vernotte C (1998) Deletion of the PB-loop in the Lcm subunit does not affect phycobilisome assembly or energy transfer functions in the cyanobacterium Synechocystis sp. PCC6714. Eur J Biochem 257:154–159

    CAS  PubMed  Google Scholar 

  • Ajlani G, Vernotte C, Dimagno L, Haselkorn R (1995) Phycobilisome Core mutants of Synechocystis PCC 6803. Biochim Biophys Acta 1231:189–196

    Google Scholar 

  • Allen JF, Sanders CE, Holmes NG (1985) Correlation of membrane-protein phosphorylation with excitation-energy distribution in the cyanobacterium Synechococcus 6301. FEBS Lett 193:271–275

    CAS  Google Scholar 

  • Aoki M, Katoh S (1982) Oxidation and reduction of plastoquinone by photosynthetic and respiratory electron transport in a cyanobacterium Synechococcus sp. Biochim Biophys Acta 682:307–314

    CAS  Google Scholar 

  • Arteni AA, Ajlani G, Boekema EJ (2009) Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim Biophys Acta 1787:272–279

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Aspinwall CL, Sarcina M, Mullineaux CW (2004) Phycobilisome mobility in the cyanobacterium Synechococcus sp. PCC7942 is influenced by the trimerisation of photosystem I. Photosynth Res 79:179–187

    CAS  PubMed  Google Scholar 

  • Bandara S, Ren Z, Lu L, Zeng X, Shin H, Zhao KH, Yang X (2017) Photoactivation mechanism of a carotenoid-based photoreceptor. Proc Natl Acad Sci U S A 114:6286–6291

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bao H, Melnicki MR, Kerfeld CA (2017a) Structure and functions of orange carotenoid protein homologs in cyanobacteria. Curr Opin Plant Biol 37:1–9

    CAS  PubMed  Google Scholar 

  • Bao H, Melnicki MR, Pawlowski EG, Sutter M, Agostoni M, Lechno-Yossef S, Cai F, Montgomery BL, Kerfeld CA (2017b) Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria. Nat Plants 3:17089

    CAS  PubMed  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    CAS  PubMed  Google Scholar 

  • Berera R, van Stokkum IH, Gwizdala M, Wilson A, Kirilovsky D, van Grondelle R (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem 116:2568–2574

    CAS  Google Scholar 

  • Berera R, Gwizdala M, van Stokkum IH, Kirilovsky D, van Grondelle R (2013) Excited states of the inactive and active forms of the orange carotenoid protein. J Phys Chem 117:9121–9128

    CAS  Google Scholar 

  • Biggins J, Bruce D (1989) Regulation of excitation-energy transfer in organisms containing phycobilins. Photosynth Res 20:1–34

    CAS  PubMed  Google Scholar 

  • Biggins J, Tanguay NA, Frank HA (1989) Electron-transfer reactions in photosystem-I following vitamin-K1 depletion by ultraviolet-irradiation. FEBS Lett 250:271–274

    CAS  PubMed  Google Scholar 

  • Billsten HH, Bhosale P, Yemelyanov A, Bernstein PS, Polivka T (2003) Photophysical properties of xanthophylls in carotenoproteins from human retinas. Photochem Photobiol 78:138–145

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Boulay C, Abasova L, Six C, Vass I, Kirilovsky D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta 1777:1344–1354

    CAS  PubMed  Google Scholar 

  • Boulay C, Wilson A, D’Haene S, Kirilovsky D (2010) Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci U S A 107:11620–11625

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bourcier de Carbon C, Thurotte A, Wilson A, Perreau F, Kirilovsky D (2015) Biosynthesis of soluble carotenoid holoproteins in Escherichia coli. Sci Rep 5:9085

    CAS  PubMed  Google Scholar 

  • Breyton C (2000) Conformational changes in the cytochrome b6f complex induced by inhibitor binding. J Biol Chem 275:13195–13201

    CAS  PubMed  Google Scholar 

  • Bruce D, Biggins J (1985) Mechanism of the light-state transition in photosynthesis : V. 77 K linear dichroism of Anacystis nidulans in state 1 and state 2. Biochim Biophys Acta 810:295–301

    CAS  Google Scholar 

  • Bruce D, Brimble S, Bryant DA (1989) State transitions in a phycobilisome-less mutant of the cyanobacterium Synechococcus sp. PCC 7002. Biochim Biophys Acta 974:66–73

    CAS  PubMed  Google Scholar 

  • Bryant DA, de Lorimier R, Guglielmi G, Stevens SE Jr (1990) Structural and compositional analyses of the phycobilisomes of Synechococcus sp. PCC 7002. Analyses of the wild-type strain and a phycocyanin-less mutant constructed by interposon mutagenesis. Arch Microbiol 153:550–560

    CAS  PubMed  Google Scholar 

  • Calzadilla PI, Zhan J, Setif P, Lemaire C, Solymosi D, Battchikova N, Wang Q, Kirilovsky D (2019) The cytochrome b6f complex is not involved in cyanobacterial state transitions. Plant Cell 31: 911–931

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Capuano V, Thomas JC, Tandeau de Marsac N, Houmard J (1993) An in vivo approach to define the role of the LCM, the key polypeptide of cyanobacterial phycobilisomes. J Biol Chem 268:8277–8283

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Zhan J, Chen Y, Yang M, He C, Ge F, Wang Q (2015) Effects of phosphorylation of beta subunits of Phycocyanins on state transition in the model cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 56:1997–2013

    CAS  PubMed  Google Scholar 

  • Chukhutsina V, Bersanini L, Aro EM, van Amerongen H (2015) Cyanobacterial light-harvesting Phycobilisomes uncouple from photosystem I during dark-to-light transitions. Sci Rep 5:14193

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Lacroix De Lavalette A, Finazzi G, Zito F (2008) b6f-Associated chlorophyll: structural and dynamic contribution to the different cytochrome functions. Biochemistry 47:5259–5265

    PubMed  Google Scholar 

  • Delphin E, Duval JC, Etienne AL, Kirilovsky D (1996) State transitions or Delta pH-dependent quenching of photosystem II fluorescence in red algae. Biochemistry 35:9435–9445

    CAS  PubMed  Google Scholar 

  • Delphin E, Duval JC, Etienne AL, Kirilovsky D (1998) Delta pH-dependent photosystem II fluorescence quenching induced by saturating, multiturnover pulses in red algae. Plant Physiol 118:103–113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    CAS  PubMed  Google Scholar 

  • Dong C, Zhao J (2008) ApcD is required for state transition but not involved in blue-light induced quenching in the cyanobacterium Anabaena sp. PCC7120. Chin Sci Bull 53:3422–3424

    CAS  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

    CAS  PubMed  Google Scholar 

  • Draber W, Trebst A, Harth E (1970) On a new inhibitor of photosynthetic electron-transport in isolated chloroplasts. Z Naturforsch B 25:1157–1159

    CAS  PubMed  Google Scholar 

  • Ducret A, Muller 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

    CAS  PubMed  Google Scholar 

  • El Bissati K, Kirilovsky D (2001) Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol 125:1988–2000

    PubMed  PubMed Central  Google Scholar 

  • El Bissati K, Delphin E, Murata N, Etienne A, Kirilovsky D (2000) Photosystem II fluorescence quenching in the cyanobacterium Synechocystis PCC 6803: involvement of two different mechanisms. Biochim Biophys Acta 1457:229–242

    PubMed  Google Scholar 

  • Elmorjani K, Thomas JC, Sebban P (1986) Phycobilisomes of wild-type and pigment mutants of the cyanobacterium Synechocystis PCC 6803. Arch Microbiol 146:186–191

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Federman S, Malkin S, Scherz A (2000) Excitation energy transfer in aggregates of photosystem I and photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: can assembly of the pigment-protein complexes control the extent of spillover? Photosynth Res 64:199–207

    CAS  PubMed  Google Scholar 

  • Finazzi G, Zito F, Barbagallo RP, Wollman FA (2001) Contrasted effects of inhibitors of cytochrome b6f complex on state transitions in Chlamydomonas reinhardtii: the role of Qo site occupancy in LHCII kinase activation. J Biol Chem 276:9770–9774

    CAS  PubMed  Google Scholar 

  • Folea IM, Zhang P, Aro EM, Boekema EJ (2008) Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. FEBS Lett 582:1749–1754

    CAS  PubMed  Google Scholar 

  • Gantt E, Conti SF (1966) Granules associated with the chloroplast lamellae of Porphyridium cruentum. J Cell Biol 29:423–434

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  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

    CAS  PubMed  Google Scholar 

  • Glazer AN (1984) Phycobilisome – a macromolecular complex optimized for light energy-transfer. Biochim Biophys Acta 768:29–51

    CAS  Google Scholar 

  • Glazer AN (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264:1–4

    CAS  PubMed  Google Scholar 

  • Gorbunov MY, Kuzminov FI, Fadeev VV, Kim JD, Falkowski PG (2011) A kinetic model of non-photochemical quenching in cyanobacteria. Biochim Biophys Acta 1807:1591–1599

    CAS  PubMed  Google Scholar 

  • Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental-conditions. Microbiol Rev 57:725–749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta S, Guttman M, Leverenz RL, Zhumadilova K, Pawlowski EG, Petzold CJ, Lee KK, Ralston CY, Kerfeld CA (2015) Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci U S A 112:E5567–E5574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gwizdala M, Wilson A, Kirilovsky D (2011) In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the orange carotenoid protein in Synechocystis PCC 6803. Plant Cell 23:2631–2643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gwizdala M, Wilson A, Omairi-Nasser A, Kirilovsky D (2013) Characterization of the Synechocystis PCC 6803 fluorescence recovery protein involved in photoprotection. Biochim Biophys Acta 1827:348–354

    CAS  PubMed  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 U S A 113:E1655–E1662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harris D, Wilson A, Muzzopappa F, Sluchanko NN, Friedrich T, Maksimov EG, Kirilovsky D, Adir N (2018) Structural rearrangements in the C-terminal domain homolog of Orange carotenoid protein are crucial for carotenoid transfer. Commun Biol 1:125

    PubMed  PubMed Central  Google Scholar 

  • Hasan SS, Yamashita E, Cramer WA (2013) Transmembrane signaling and assembly of the cytochrome b6f-lipidic charge transfer complex. Biochim Biophys Acta 1827:1295–1308

    CAS  PubMed Central  Google Scholar 

  • Holt TK, Krogmann DW (1981) A carotenoid-protein from cyanobacteria. Biochim Biophys Acta 637:408–414

    CAS  Google Scholar 

  • Huang C, Yuan X, Zhao J, Bryant DA (2003) Kinetic analyses of state transitions of the cyanobacterium Synechococcus sp. PCC 7002 and its mutant strains impaired in electron transport. Biochim Biophys Acta 1607:121–130

    CAS  PubMed  Google Scholar 

  • Jallet D, Gwizdala M, Kirilovsky D (2012) 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 1817:1418–1427

    CAS  PubMed  Google Scholar 

  • Jallet D, Thurotte A, Leverenz RL, Perreau F, Kerfeld CA, Kirilovsky D (2014) Specificity of the cyanobacterial orange carotenoid protein: influences of orange carotenoid protein and phycobilisome structures. Plant Physiol 164:790–804

    CAS  PubMed  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917

    CAS  PubMed  Google Scholar 

  • Joshua S, Mullineaux CW (2004) Phycobilisome diffusion is required for light-state transitions in cyanobacteria. Plant Physiol 135:2112–2119

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joshua S, Mullineaux CW (2005) The rpaC gene product regulates phycobilisome-photosystem II interaction in cyanobacteria. Biochim Biophys Acta 1709:58–68

    CAS  PubMed  Google Scholar 

  • Kana R (2013) Mobility of photosynthetic proteins. Photosynth Res 116:465–479

    CAS  PubMed  Google Scholar 

  • Kana R, Prasil O, Komarek O, Papageorgiou GC (2009) Govindjee, spectral characteristic of fluorescence induction in a model cyanobacterium, Synechococcus sp. PCC 7942. Biochim Biophys Acta 1787:1170–1178

    CAS  PubMed  Google Scholar 

  • Kana R, Kotabova E, Komarek O, Sediva B, Papageorgiou GC, Govindjee OP (2012) The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta 1817:1237–1247

    CAS  PubMed  Google Scholar 

  • Kana R, Kotabova E, Lukes M, Papacek S, Matonoha C, Liu LN, Prasil O, Mullineaux CW (2014) Phycobilisome mobility and its role in the regulation of light harvesting in red algae. Plant Physiol 165:1618–1631

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karapetyan NV (2007) Non-photochemical quenching of fluorescence in cyanobacteria. Biochemistry 72:1127–1135

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kerfeld CA (2004b) Water-soluble carotenoid proteins of cyanobacteria. Arch Biochem Biophys 430:2–9

    CAS  PubMed  Google Scholar 

  • Kerfeld CA, Kirilovsky D (2013) Structural, mechanistic and genomic insights into OCP-mediated photoprotection. In: Chauvat F, Cassier-Chauvat C (eds) Advances in botanical research: genomics in cyanobacteria. Elsevier, Oxford, pp 1–26

    Google Scholar 

  • Kerfeld CA, Sawaya MR, Brahmandam V, Cascio D, Ho KK, Trevithick-Sutton CC, Krogmann DW, Yeates TO (2003) The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11:55–65

    CAS  PubMed  Google Scholar 

  • Kerfeld CA, Alexandre M, Kirilovsky D (2009) The orange carotenoid protein in cyanobacteria. In: Landrum J (ed) Carotenoids: Physical, chemical and biological functions and properties. Taylor and Francis group, Boca Raton, pp 3–19

    Google Scholar 

  • Kerfeld CA, Melnicki MR, Sutter M, Dominguez-Martin MA (2017) Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. New Phytol 215:937–951

    CAS  PubMed  Google Scholar 

  • Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16

    CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817:158–166

    CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2013) The orange carotenoid protein: a blue-green light photoactive protein. Photochem Photobiol Sci 12:1135–1143

    CAS  PubMed  Google Scholar 

  • Kirilovsky D, Kana R, Prasil O (2014) Mechanisms modulating energy arriving at reaction centers in cyanobacteria. In: Demmig-Adams B, Garab G, Adams W, Govindjee (eds) Non-Photochemical Quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Dordrecht/Heidelberg/New York/London, pp 471–501

    Google Scholar 

  • Kish E, Kos PB, Chen M, Vass I (2015a) A unique regulation of the expression of the psbA, psbD, and psbE genes, encoding the 01, 02 and cytochrome b559 subunits of the photosystem II complex in the chlorophyll d containing cyanobacterium Acaryochloris marina. Biochim Biophys Acta 1817:1083–1094

    Google Scholar 

  • Kish E, Pinto MM, Kirilovsky D, Spezia R, Robert B (2015b) Echinenone vibrational properties: from solvents to the orange carotenoid protein. Biochim Biophys Acta 1847:1044–1054

    CAS  PubMed  Google Scholar 

  • Kondo K, Geng XX, Katayama M, Ikeuchi M (2005) Distinct roles of CpcG1 and CpcG2 in phycobilisome assembly in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 84:269–273

    CAS  PubMed  Google Scholar 

  • Kondo K, Ochiai Y, Katayama M, Ikeuchi M (2007) The membrane-associated CpcG2-phycobilisome in Synechocystis: a new photosystem I antenna. Plant Physiol 144:1200–1210

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kondo K, Mullineaux CW, Ikeuchi M (2009) Distinct roles of CpcG1-phycobilisome and CpcG2-phycobilisome in state transitions in a cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res 99:217–225

    CAS  PubMed  Google Scholar 

  • Konold PE, van Stokkum IHM, Muzzopappa F, Wilson A, Groot M-L, Kirilovsky D and Kennis JTM (2019) Photoactivation mechanism, timing of protein secondary structure dynamics and carotenoid translocation in the Orange carotenoid protein. J Am Chem Soc J Am Chem Soc 141:520–530

    Google Scholar 

  • Krupnik T, Kotabova E, van Bezouwen LS, Mazur R, Garstka M, Nixon PJ, Barber J, Kana R, Boekema EJ, Kargul J (2013) A reaction center-dependent photoprotection mechanism in a highly robust photosystem II from an extremophilic red alga, Cyanidioschyzon merolae. J Biol Chem 288:23529–23542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzminov FI, Karapetyan NV, Rakhimberdieva MG, Elanskaya IV, Gorbunov MY, Fadeev VV (2012) Investigation of OCP-triggered dissipation of excitation energy in PSI/PSII-less Synechocystis sp. PCC 6803 mutant using non-linear laser fluorimetry. Biochim Biophys Acta 1817:1012–1021

    CAS  PubMed  Google Scholar 

  • Lechno-Yossef S, Melnicki MR, Bao H, Montgomery BL, Kerfeld CA (2017) Synthetic OCP heterodimers are photoactive and recapitulate the fusion of two primitive carotenoproteins in the evolution of cyanobacterial photoprotection. Plant J 91:646–656

    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 26:426–437

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ley AC, Butler WL (1980) Energy distribution in the photochemical apparatus of Porphyridium cruentum in state-I and state-II. Biochim Biophys Acta 592:349–363

    CAS  PubMed  Google Scholar 

  • Li Y, Zhang J, Xie J, Zhao J, Jiang L (2001) Temperature-induced decoupling of phycobilisomes from reaction centers. Biochim Biophys Acta 1504:229–234

    CAS  PubMed  Google Scholar 

  • Li D, Xie J, Zhao J, Xia A, Li D, Gong Y (2004) Light-induced excitation energy redistribution in Spirulina platensis cells: “spillover” or “mobile PBSs”. Biochim Biophys Acta 1608:114–121

    CAS  PubMed  Google Scholar 

  • Li H, Li D, Yang S, Xie J, Zhao J (2006) The state transition mechanism – simply depending on light-on and -off in Spirulina platensis. Biochim Biophys Acta 1757:1512–1519

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  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 342:1104–1107

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Zhang H, King JD, Wolf NR, Prado M, Gross ML, Blankenship RE (2014) Mass spectrometry footprinting reveals the structural rearrangements of cyanobacterial orange carotenoid protein upon light activation. Biochim Biophys Acta 1837:1955–1963

    CAS  PubMed  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 55:1003–1009

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Igual R, Wilson A, Leverenz RL, Melnicki MR, Bourcier de Carbon C, Sutter M, Turmo A, Perreau F, Kerfeld CA, Kirilovsky D (2016) Different functions of the Paralogs to the N-terminal domain of the orange carotenoid protein in the Cyanobacterium Anabaena sp. PCC 7120. Plant Physiol 171:1852–1866

    PubMed  PubMed Central  Google Scholar 

  • Lu Y, Liu H, Saer R, Li VL, Zhang H, Shi L, Goodson C, Gross ML, Blankenship RE (2017a) A molecular mechanism for nonphotochemical quenching in cyanobacteria. Biochemistry 56:2812–2823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Liu H, Saer RG, Zhang H, Meyer CM, Li VL, Shi L, King JD, Gross ML, Blankenship RE (2017b) Native mass spectrometry analysis of Oligomerization states of fluorescence recovery protein and orange carotenoid protein: two proteins involved in the cyanobacterial photoprotection cycle. Biochemistry 56:160–166

    CAS  PubMed  Google Scholar 

  • Ludwig M, Bryant DA (2011) Transcription profiling of the model cyanobacterium Synechococcus sp strain PCC 7002 by next-gen (SOLiD™) sequencing of cDNA. Front Microbiol 2(41). https://doi.org/10.3389/fmicb.2011.00041

  • Ludwig M, Bryant DA (2012) Acclimation of the global transcriptome of the cyanobacterium sp strain PCC 7002 to nutrient limitations and different nitrogen sources. Front Microbiol 3:145. https://doi.org/10.3389/fmicb.2012.00145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334

    CAS  PubMed  Google Scholar 

  • Maksimov EG, Shirshin EA, Sluchanko NN, Zlenko DV, Parshina EY, Tsoraev GV, Klementiev KE, Budylin GS, Schmitt FJ, Friedrich T, Fadeev VV, Paschenko VZ, Rubin AB (2015a) The signaling state of orange carotenoid protein. Biophys J 109:595–607

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maksimov EG, Klementiev KE, Shirshin EA, Tsoraev GV, Elanskaya IV, Paschenko VZ (2015b) Features of temporal behavior of fluorescence recovery in Synechocystis sp. PCC6803. Photosynth Res 125:167–178

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Maksimov EG, Sluchanko NN, Mironov KS, Shirshin EA, Klementiev KE, Tsoraev GV, Moldenhauer M, Friedrich T, Los DA, Allakhverdiev SI, Paschenko VZ, Rubin AB (2017a) Fluorescent labeling preserving OCP photoactivity reveals its reorganization during the photocycle. Biophys J 112:46–56

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maksimov EG, Sluchanko NN, Slonimskiy YB, Slutskaya EA, Stepanov AV, Argentova-Stevens AM, Shirshin EA, Tsoraev GV, Klementiev KE, Slatinskaya OV, Lukashev EP, Friedrich T, Paschenko VZ, Rubin AB (2017b) The photocycle of orange carotenoid protein conceals distinct intermediates and asynchronous changes in the carotenoid and protein components. Sci Rep 7:15548

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mao HB, Li GF, Ruan X, Wu QY, Gong YD, Zhang XF, Zhao NM (2002) The redox state of plastoquinone pool regulates state transitions via cytochrome b6f complex in Synechocystis sp. PCC 6803. FEBS Lett 519:82–86

    CAS  PubMed  Google Scholar 

  • Mao L, Wang Y, Hu X (2003) pi-pi stacking interactions in the peridinin-chlorophyll-protein of Amphidinium carterae. J Phys Chem B 107:3963–3971

    CAS  Google Scholar 

  • McConnell MD, Koop R, Vasil’ev S, Bruce D (2002) Regulation of the distribution of chlorophyll and phycobilin-absorbed excitation energy in cyanobacteria. A structure-based model for the light state transition. Plant Physiol 130:1201–1212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Melnicki MR, Leverenz RL, Sutter M, Lopez-Igual R, Wilson A, Pawlowski EG, Perreau F, Kirilovsky D, Kerfeld CA (2016) Structure, diversity, and evolution of a new family of soluble carotenoid-binding proteins in cyanobacteria. Mol Plant 9:1379–1394

    CAS  PubMed  Google Scholar 

  • Misumi M, Katoh H, Tomo T, Sonoike K (2016) Relationship between photochemical quenching and non-photochemical quenching in six species of cyanobacteria reveals species difference in redox state and species commonality in energy dissipation. Plant Cell Physiol 57:1510–1517

    CAS  PubMed  Google Scholar 

  • Moldenhauer M, Sluchanko NN, Tavraz NN, Junghans C, Buhrke D, Willoweit M, Chiappisi L, Schmitt FJ, Vukojevic V, Shirshin EA, Ponomarev VY, Paschenko VZ, Gradzielski M, Maksimov EG, Friedrich T (2018) Interaction of the signaling state analog and the apoprotein form of the orange carotenoid protein with the fluorescence recovery protein. Photosynth Res 135:125–139

    CAS  PubMed  Google Scholar 

  • Mullineaux CW (1992) Excitation energy transfer from phycobilisomes to photosystem-I and photosystem-II in a Cyanobacterium. Photosynth Res 34:114–114

    Google Scholar 

  • Mullineaux CW (2008) Factors controlling the mobility of photosynthetic proteins. Photochem Photobiol 84:1310–1316

    CAS  PubMed  Google Scholar 

  • Mullineaux CW (2014) Co-existence of photosynthetic and respiratory activities in cyanobacterial thylakoid membranes. Biochim Biophys Acta 1837:503–511

    CAS  PubMed  Google Scholar 

  • Mullineaux CW, Allen JF (1986) The state 2 transition in the cyanobacterium Synechococcus 6301 can be driven by respiratory electron flow into the plastoquinone pool. FEBS Lett 205:155–160

    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 photosystem I and photosystem II. Photosynth Res 23:297–311

    CAS  PubMed  Google Scholar 

  • Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393

    CAS  PubMed  Google Scholar 

  • Mullineaux CW, Tobin MJ, Jones GR (1997) Mobility of photosynthetic complexes in thylakoid membranes. Nature 390:421–424

    CAS  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 172:242–251

    CAS  PubMed  Google Scholar 

  • Muzzopappa F, Wilson A, Yogarajah V, Cot S, Perreau F, Montigny C, Bourcier de Carbon C, Kirilovsky D (2017) Paralogs of the C-terminal domain of the Cyanobacterial Orange carotenoid protein are carotenoid donors to helical carotenoid proteins. Plant Physiol 175:1283–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muzzopappa F, Wilson A, Kirilovsky D (2019) Interdomain interactions reveal the molecular evolution of the Orange carotenoid protein. Nat Plants 5:1076–1086

    Google Scholar 

  • Nanba M, Katoh S (1985) Restoration by tetramethyl-p-phenylenediamine of photosynthesis in dibromothymoquinone-inhibited cells of the cyanobacterium Synechococcus sp. Biochim Biophys Acta 809:74–80

    CAS  Google Scholar 

  • Niedzwiedzki DM, Liu H, Blankenship RE (2014) Excited state properties of 3′-hydroxyechinenone in solvents and in the orange carotenoid protein from Synechocystis sp. PCC 6803. J Phys Chem 118:6141–6149

    CAS  Google Scholar 

  • Ogawa T, Sonoike K (2015) Dissection of respiration and photosynthesis in the cyanobacterium Synechocystis sp. PCC6803 by the analysis of chlorophyll fluorescence. J Photochem Photobiol 144:61–67

    CAS  Google Scholar 

  • Olive J, Mbina I, Vernotte C, Astier C, Wollman FA (1986) Randomization of the Ef particles in thylakoid membranes of Synechocystis 6714 upon transition from state-I to state-II. FEBS Lett 208:308–312

    CAS  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 1319:275–282

    CAS  Google Scholar 

  • Polivka T, Kerfeld CA, Pascher T, Sundström V (2005) Spectroscopic properties of the carotenoid 3′-hydroxyechinenone in the orange carotenoid protein from the cyanobacterium Arthrospira maxima. Biochemistry 44:3994–4003

    CAS  PubMed  Google Scholar 

  • Polivka T, Chabera P, Kerfeld CA (2013) Carotenoid-protein interaction alters the S(1) energy of hydroxyechinenone in the orange carotenoid protein. Biochim Biophys Acta 1827:248–254

    CAS  PubMed  Google Scholar 

  • Punginelli C, Wilson A, Routaboul JM, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the orange carotenoid protein. Biochim Biophys Acta 1787:280–288

    CAS  PubMed  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 40:15780–15788

    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. FEBS Lett 574:85–88

    CAS  PubMed  Google Scholar 

  • Rakhimberdieva MG, Elanskaya IV, Vermaas WFJ, Karapetyan NV (2010) Carotenoid-triggered energy dissipation in phycobilisomes of Synechocystis sp. PCC 6803 diverts excitation away from reaction centers of both photosystems. Biochim Biophys Acta 1797:241–249

    CAS  PubMed  Google Scholar 

  • Ranjbar Choubeh R, Wientjes E, Struik PC, Kirilovsky D, van Amerongen H (2018) State transitions in the cyanobacterium Synechococcus elongatus 7942 involve reversible quenching of the photosystem II core. Biochim Biophys Acta 1859:1059–1066

    CAS  Google Scholar 

  • Redlinger T, Gantt E (1982) A M(r) 95,000 polypeptide in Porphyridium cruentum phycobilisomes and thylakoids: possible function in linkage of phycobilisomes to thylakoids and in energy transfer. Proc Natl Acad Sci U S A 79:5542–5546

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reuter W, Wiegand G, Huber R, Than ME (1999) Structural analysis at 2.2 angstrom of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP center dot L-C(7.8), from phycobilisomes of Mastigocladus laminosus. Proc Natl Acad Sci U S A 96:1363–1368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H (2007a) Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. Plant Physiol 144:1336–1346

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakurai I, Mizusawa N, Wada H, Sato N (2007b) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 145:1361–1370

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarcina M, Mullineaux CW (2004) Mobility of the IsiA chlorophyll-binding protein in cyanobacterial thylakoid membranes. J Biol Chem 279:36514–36518

    CAS  PubMed  Google Scholar 

  • Sarcina M, Tobin MJ, Mullineaux CW (2001) Diffusion of phycobilisomes on the thylakoid membranes of the cyanobacterium Synechococcus 7942. Effects of phycobilisome size, temperature, and membrane lipid composition. J Biol Chem 276:46830–46834

    CAS  PubMed  Google Scholar 

  • Schluchter WM, Shen GH, Zhao JD, Bryant DA (1996) Characterization of psaI and psaL mutants of Synechococcus sp strain PCC 7002: a new model for state transitions in cyanobacteria. Photochem Photobiol 64:53–66

    CAS  PubMed  Google Scholar 

  • Scott M, McCollum C, Vasil’ev S, Crozier C, Espie GS, Krol M, Huner NP, Bruce D (2006) Mechanism of the down regulation of photosynthesis by blue light in the Cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 45:8952–8958

    CAS  PubMed  Google Scholar 

  • Shen G, Boussiba S, Vermaas WF (1993) Synechocystis sp PCC 6803 strains lacking photosystem I and phycobilisome function. Plant Cell 5:1853–1863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh AK, Bhattacharyya-Pakrasi M, Elvitigala T, Ghosh B, Aurora R, Pakrasi HB (2009) A systems-level analysis of the effects of light quality on the metabolism of a cyanobacterium. Plant Physiol 151:1596–1608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Slonimskiy YB, Maksimov EG, Lukashev EP, Moldenhauer M, Jeffries CM, Svergun DI, Friedrich T, Sluchanko NN (2018) Functional interaction of low-homology FRPs from different cyanobacteria with Synechocystis OCP. Biochim Biophys Acta 1859:382–393

    CAS  Google Scholar 

  • Slouf V, Kuznetsova V, Fuciman M, de Carbon CB, Wilson A, Kirilovsky D, Polivka T (2017) Ultrafast spectroscopy tracks carotenoid configurations in the orange and red carotenoid proteins from cyanobacteria. Photosynth Res 131:105–117

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Klementiev KE, Shirshin EA, Tsoraev GV, Friedrich T, Maksimov EG (2017a) The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP. Biochim Biophys Acta 1858:1–11

    CAS  Google Scholar 

  • Sluchanko NN, Slonimskiy YB, Moldenhauer M, Friedrich T, Maksimov EG (2017b) Deletion of the short N-terminal extension in OCP reveals the main site for FRP binding. FEBS Lett 591:1667–1676

    CAS  PubMed  Google Scholar 

  • Sluchanko NN, Slonimskiy YB, Shirshin EA, Moldenhauer M, Friedrich T, Maksimov EG (2018) OCP-FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria. Nat Commun 9:3869

    PubMed  PubMed Central  Google Scholar 

  • Spat P, Macek B, Forchhammer K (2015) Phosphoproteome of the cyanobacterium Synechocystis sp. PCC 6803 and its dynamics during nitrogen starvation. Front Microbiol 6:248

    PubMed  PubMed Central  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 1917:1436–1445

    Google Scholar 

  • Steinbach G, Schubert F, Kana R (2015) Cryo-imaging of photosystems and phycobilisomes in Anabaena sp. PCC 7120 cells. J Photochem Photobiol 152 (395–399

    Google Scholar 

  • Stoitchkova K, Zsiros O, Javorfi T, Pali T, Andreeva A, Gombos Z, Garab G (2007) Heat- and light-induced reorganizations in the phycobilisome antenna of Synechocystis sp. PCC 6803. Thermo-optic effect. Biochim Biophys Acta 1767:750–756

    CAS  PubMed  Google Scholar 

  • Straub C, Quillardet P, Vergalli J, de Marsac NT, Humbert JF (2011) A day in the life of microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS One 6:e16208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418

    CAS  PubMed  Google Scholar 

  • Sutter M, Wilson A, Leverenz RL, Lopez-Igual R, Thurotte A, Salmeen AE, Kirilovsky D, Kerfeld CA (2013) Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci U S A 110:10022–10027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tandeau de Marsac N (2003) Phycobiliproteins and phycobilisomes: the early observations. Photosynth Res 76:197–205

    CAS  Google Scholar 

  • Thurotte A, Lopez-Igual R, Wilson A, Comolet L, Bourcier de Carbon C, Xiao F, Kirilovsky D (2015) Regulation of Orange carotenoid protein activity in cyanobacterial photoprotection. Plant Physiol 169:737–747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thurotte A, Bourcier de Carbon C, Wilson A, Talbot L, Cot S, Lopez-Igual R, Kirilovsky D (2017) The cyanobacterial fluorescence recovery protein has two distinct activities: orange carotenoid protein amino acids involved in FRP interaction. Biochim Biophys Acta Bioenerg 1858:308–317

    CAS  PubMed  Google Scholar 

  • Tian L, van Stokkum IH, Koehorst RB, Jongerius A, Kirilovsky D, van Amerongen H (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133:18304–18311

    CAS  PubMed  Google Scholar 

  • Tian L, Gwizdala M, van Stokkum IH, Koehorst RB, Kirilovsky D, van Amerongen H (2012) Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J 102:1692–1700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473:55–60

    CAS  PubMed  Google Scholar 

  • Veerman J, Bentley FK, Eaton-Rye JJ, Mullineaux CW, Vasil’ev S, Bruce D (2005) The PsbU subunit of photosystem II stabilizes energy transfer and primary photochemistry in the phycobilisome-photosystem II assembly of Synechocystis sp. PCC 6803. Biochemistry 44:16939–16948

    CAS  PubMed  Google Scholar 

  • Vener AV, Van Kan PJ, Gal A, Andersson B, Ohad I (1995) Activation/deactivation cycle of redox-controlled thylakoid protein phosphorylation. Role of plastoquinol bound to the reduced cytochrome bf complex. J Biol Chem 270:25225–25232

    CAS  PubMed  Google Scholar 

  • Vener AV, van Kan PJ, Rich PR, Ohad I, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci U S A 94:1585–1590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vernotte C, Picaud M, Kirilovsky D, Olive J, Ajlani G, Astier C (1992) Changes in the photosynthetic apparatus in the cyanobacterium Synechocystis sp PCC 6714 following light-to-dark and dark-to-light transitions. Photosynth Res 32:45–57

    CAS  PubMed  Google Scholar 

  • Vladkova R (2016) Chlorophyll a is the crucial redox sensor and transmembrane signal transmitter in the cytochrome b6f complex. Components and mechanisms of state transitions from the hydrophobic mismatch viewpoint. J Biomol Struct Dyn 34:824–854

    CAS  PubMed  Google Scholar 

  • Wang Q, Moerner WE (2015) Dissecting pigment architecture of individual photosynthetic antenna complexes in solution. Proc Natl Acad Sci U S A 112:13880–13885

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • 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 U S A 111:2512–2517

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams RC, Gingrich JC, Glazer AN (1980) Cyanobacterial phycobilisomes. Particles from Synechocystis 6701 and two pigment mutants. J Cell Biol 85:558–566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson A, Boulay C, Wilde A, Kerfeld CA, Kirilovsky D (2007) Light-induced energy dissipation in iron-starved cyanobacteria: roles of OCP and IsiA proteins. Plant Cell 19:656–672

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson A, Punginelli C, Gall A, Bonetti C, Alexandre M, Routaboul JM, Kerfeld CA, van Grondelle R, Robert B, Kennis JT, Kirilovsky D (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci U S A 105:12075–12080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson A, Kinney JN, Zwart PH, Punginelli C, D’Haene S, Perreau F, Klein MG, Kirilovsky D, Kerfeld CA (2010) Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J Biol Chem 285:18364–18375

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson A, Punginelli C, Couturier M, Perrau F, Kirilovsky D (2011) Essential role of two tyrosines and two tryptophans on photoprotection activity of the orange carotenoid protein. Biochim Biophys Acta 1807:293–301

    CAS  PubMed  Google Scholar 

  • Wilson A, Gwizdala M, Mezzetti A, Alexandre M, Kerfeld CA, Kirilovsky D (2012) The essential role of the N-terminal domain of the orange carotenoid protein in cyanobacterial photoprotection: importance of a positive charge for phycobilisome binding. Plant Cell 24:1972–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wollman FA, Lemaire C (1988) Studies on kinase-controlled state transitions in photosystem II and b6f mutants from Chlamydomonas reinhardtii which lack quinone-binding proteins. Biochim Biophys Acta 933:85–94

    CAS  Google Scholar 

  • Wu YP, Krogmann DW (1997) The orange carotenoid protein of Synechocystis PCC 6803. Biochim Biophys Acta 1322:1–7

    CAS  PubMed  Google Scholar 

  • Yamanaka G, Glazer AN, Williams RC (1978) Cyanobacterial phycobilisomes. Characterization of the phycobilisomes of Synechococcus sp. 6301. J Biol Chem 253:8303–8310

    CAS  PubMed  Google Scholar 

  • Yang S, Su Z, Li H, Feng J, Xie J, Xia A, Gong Y, Zhao J (2007) Demonstration of phycobilisome mobility by the time- and space-correlated fluorescence imaging of a cyanobacterial cell. Biochim Biophys Acta 1767:15–21

    CAS  PubMed  Google Scholar 

  • Yang S, Zhang R, Hu C, Xie J, Zhao J (2009) The dynamic behavior of phycobilisome movement during light state transitions in cyanobacterium Synechocystis PCC6803. Photosynth Res 99:99–106

    CAS  PubMed  Google Scholar 

  • Yang MK, Qiao ZX, Zhang WY, Xiong Q, Zhang J, Li T, Ge F, Zhao JD (2013) Global phosphoproteomic analysis reveals diverse functions of serine/threonine/tyrosine phosphorylation in the model cyanobacterium Synechococcus sp. strain PCC 7002. J Proteome Res 12:1909–1923

    CAS  PubMed  Google Scholar 

  • Yu MH, Glazer AN (1982) Cyanobacterial phycobilisomes. Role of the linker polypeptides in the assembly of phycocyanin. J Biol Chem 257:3429–3433

    CAS  PubMed  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392:677–684

    CAS  PubMed  Google Scholar 

  • Zhang H, Liu H, Niedzwiedzki DM, Prado M, Jiang J, Gross ML, Blankenship RE (2013) Molecular mechanism of photoactivation and structural location of the cyanobacterial orange carotenoid protein. Biochemistry 53:13–19

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao JD, Zhou JH, Bryant DA (1992) Energy transfer processes in phycobilisomes as deduced from mutational analyses. Photosynth Res 34:83–83

    Google Scholar 

  • Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2969

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Integrative Biology of the Cell (I2BC), CNRS, CEA, Université Paris-Sud, Université Paris-Saclay, Gif sur Yvette, France

    Diana Kirilovsky

Authors
  1. Diana Kirilovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diana Kirilovsky .

Editor information

Editors and Affiliations

  1. Global Climate Custer, University of Technology Sydney, Ultimo, NSW, Australia

    Anthony W.D. Larkum

  2. Department of Plant Biology, Carnegie Institution for Science, Stanford University, Stanford, CA, USA

    Arthur R. Grossman

  3. Division of Plant Sciences, University of Dundee at the JHI, Dundee, UK

    John A. Raven

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Kirilovsky, D. (2020). Modulating Energy Transfer from Phycobilisomes to Photosystems: State Transitions and OCP-Related Non-Photochemical Quenching. In: Larkum, A., Grossman, A., Raven, J. (eds) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Advances in Photosynthesis and Respiration, vol 45. Springer, Cham. https://doi.org/10.1007/978-3-030-33397-3_14

Download citation

Publish with us

Policies and ethics

Search

Navigation