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Conversion of photosystem II dimer to monomers during photoinhibition is tightly coupled with decrease in oxygen-evolving activity in the diatom Chaetoceros gracilis

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Abstract

The rapid turnover of photosystem II (PSII) in diatoms is thought to be at an exceptionally high rate compared with other oxyphototrophs; however, its molecular mechanisms are largely unknown. In this study, we examined the photodamage and repair processes of PSII in the marine centric diatom Chaetoceros gracilis incubated at 30 or 300 μmol photons m−2 s−1 in the presence of a de novo protein-synthesis inhibitor. When de novo protein synthesis was blocked by chloramphenicol (Cm), oxygen-evolving activity gradually decreased even at 30 μmol photons m−2 s−1 and could not be detected at 12 h. PSII inactivation was enhanced by higher illumination. Using Cm-treated cells, the conversion of PSII dimer to monomers was observed by blue native PAGE. The rate of PSII monomerization was very similar to that of the decrease in oxygen-evolving activity under both light conditions. Immunological detection of D1 protein in the Cm-treated cells showed that the rate of D1 degradation was slower than that of the former two events, although it was more rapid than that observed in other oxyphototrophs. Thus, the three accelerated events, especially PSII monomerization, appear to cause the unusually high rate of PSII turnover in diatoms.

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Abbreviations

BN-PAGE:

Blue native PAGE

Chl:

Chlorophyll

Cm:

Chloramphenicol

FCP:

Fucoxanthin chlorophyll a/c-binding protein

HL:

High light

LL:

Low light

MES:

2-(N-morpholino)ethanesulfonic acid

PS:

Photosystem

RC:

Reaction center

RubisCO:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

References

  • Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of Photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32

    Article  CAS  PubMed  Google Scholar 

  • Anderson JM, Chow WS (2002) Structural and functional dynamics of plant photosystem II. Philos Trans R Soc Lond B Biol Sci 357:1421–1430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  CAS  PubMed  Google Scholar 

  • Aro E-M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356

    Article  CAS  PubMed  Google Scholar 

  • Bentley FK, Luo H, Dilbeck P, Burnap RL, Eaton-Rye JJ (2008) Effects of inactivating psbM and psbT on photodamage and assembly of photosystem II in Synechocystis sp. PCC 6803. Biochemistry 47:11637–11646

    Article  CAS  PubMed  Google Scholar 

  • Bidle KD (2015) The molecular ecophysiology of programmed cell death in marine phytoplankton. Ann Rev Mar Sci 7:341–375

    Article  PubMed  Google Scholar 

  • Chi W, Sun X, Zhang L (2012) The roles of chloroplast proteases in the biogenesis and maintenance of photosystem II. Biochim Biophys Acta 1817:239–246

    Article  CAS  PubMed  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102:269–352

    Article  CAS  PubMed  Google Scholar 

  • Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  • Grundmeier A, Dau H (2012) Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim Biophys Acta 1817:88–105

    Article  CAS  PubMed  Google Scholar 

  • Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    Article  CAS  PubMed  Google Scholar 

  • Hankamer B, Nield J, Zheleva D, Boekema E, Jansson S, Barber J (1997) Isolation and biochemical characterisation of monomeric and dimeric photosystem II complexes from spinach and their relevance to the organisation of photosystem II in vivo. Eur J Biochem 243:422–429

    Article  CAS  PubMed  Google Scholar 

  • Hillier W, Messinger J (2005) Mechanism of photosynthetic oxygen production. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, pp 567–608

    Google Scholar 

  • Ifuku K, Yan D, Miyahara M, Inoue-Kashino N, Yamamoto YY, Kashino Y (2014) A stable and efficient nuclear transformation system for the diatom Chaetoceros gracilis. Photosynth Res 123:203–211

    Article  PubMed  Google Scholar 

  • Ikeda Y, Komura M, Watanabe M, Minami C, Koike H, Itoh S, Kashino Y, Satoh K (2008) Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1777:351–361

    Article  CAS  PubMed  Google Scholar 

  • Ikeuchi M, Inoue Y (1988) A new photosystem II reaction center component (4.8 kDa protein) encoded by chloroplast genome. FEBS Lett 241:99–104

    Article  CAS  PubMed  Google Scholar 

  • Ishihara T, Ifuku K, Yamashita E, Fukunaga Y, Nishino Y, Miyazawa A, Kashino Y, Inoue-Kashino N (2015) Utilization of light by fucoxanthin-chlorophyll-binding protein in a marine centric diatom, Chaetoceros gracilis. Photosynth Res 126:437–447

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Katoh H, Katayama M, Ikeuchi M (2004) PSII-Tc protein plays an important role in dimerization of photosystem II. Plant Cell Physiol 45:1809–1816

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    CAS  Google Scholar 

  • Kato Y, Sakamoto W (2010) New insights into the types and function of proteases in plastids. Int Rev Cell Mol Biol 280:185–218

    Article  CAS  PubMed  Google Scholar 

  • Kern J, Loll B, Lüneberg C, DiFiore D, Biesiadka J, Irrgang K-D, Zouni A (2005) Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim Biophys Acta 1706:147–157

    Article  CAS  PubMed  Google Scholar 

  • Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12:95–104

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Nickelsen J, Tichý M, Prášil O, Eichacker LA, Nixon PJ (2008) The cyanobacterial homologue of HCF136/YCF48 is a component of an early photosystem II assembly complex and is important for both the efficient assembly and repair of photosystem II in Synechocystis sp. PCC 6803. J Biol Chem 283:22390–22399

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Sobotka R, Nixon PJ (2012) Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15:245–251

    Article  CAS  PubMed  Google Scholar 

  • Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, Schmid GH, Barber J (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem 275:6509–6514

    Article  CAS  PubMed  Google Scholar 

  • MacIntyre HL, Kana TM, Geider RJ (2000) The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends Plant Sci 5:12–17

    Article  CAS  PubMed  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483

    Article  CAS  PubMed  Google Scholar 

  • Messinger J, Noguchi T, Yano J (2012) Photosynthetic O2 evolution. In: Wydrzynski TJ, Hillier W (eds) Molecular solar fuels. Royal Society of Chemistry, Cambridge, pp 163–207

    Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Ishii A, Tada O, Suzuki T, Dohmae N, Okumura A, Iwai M, Takahashi T, Kashino Y, Enami I (2007) Isolation and characterization of oxygen-evolving thylakoid membranes and Photosystem II particles from a marine diatom Chaetoceros gracilis. Biochim Biophys Acta 1767:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Moriguchi A, Tomo T, Niikura A, Nakajima S, Suzuki T, Okumura A, Iwai M, Shen J-R, Ikeuchi M, Enami I (2010a) Binding and functional properties of five extrinsic proteins in oxygen-evolving photosystem II from a marine centric diatom, Chaetoceros gracilis. J Biol Chem 285:29191–29199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagao R, Tomo T, Noguchi E, Nakajima S, Suzuki T, Okumura A, Kashino Y, Mimuro M, Ikeuchi M, Enami I (2010b) Purification and characterization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1797:160–166

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Tomo T, Noguchi E, Suzuki T, Okumura A, Narikawa R, Enami I, Ikeuchi M (2012) Proteases are associated with a minor fucoxanthin chlorophyll a/c-binding protein from the diatom, Chaetoceros gracilis. Biochim Biophys Acta 1817:2110–2117

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Suga M, Niikura A, Okumura A, Koua FHM, Suzuki T, Tomo T, Enami I, Shen J-R (2013a) Crystal structure of Psb31, a novel extrinsic protein of photosystem II from a marine centric diatom and implications for its binding and function. Biochemistry 52:6646–6652

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Takahashi S, Suzuki T, Dohmae N, Nakazato K, Tomo T (2013b) Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species. Photosynth Res 117:281–288

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Tomo T, Narikawa R, Enami I, Ikeuchi M (2013c) Light-independent biosynthesis and assembly of the photosystem II complex in the diatom Chaetoceros gracilis. FEBS Lett 587:1340–1345

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Akimoto S, Tomo T (2013d) High excitation energy quenching in fucoxanthin chlorophyll a/c-binding protein complexes from the diatom Chaetoceros gracilis. J Phys Chem B 117:6888–6895

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Teshigahara A, Akimoto S, Tomo T (2014a) Light-harvesting ability of the fucoxanthin chlorophyll a/c-binding protein associated with photosystem II from the diatom Chaetoceros gracilis as revealed by picosecond time-resolved fluorescence spectroscopy. J Phys Chem B 118:5093–5100

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Tomo T, Akimoto S (2014b) Control mechanism of excitation energy transfer in a complex consisting of photosystem II and fucoxanthin chlorophyll a/c-binding protein. J Phys Chem Lett 5:2983–2987

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20:5587–5594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  CAS  PubMed  Google Scholar 

  • Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106:1–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohnishi N, Takahashi Y (2001) PsbT polypeptide is required for efficient repair of photodamaged photosystem II reaction center. J Biol Chem 276:33798–33804

    Article  CAS  PubMed  Google Scholar 

  • Pospíšil P (2012) Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochim Biophys Acta 1817:218–231

    Article  PubMed  Google Scholar 

  • Renger G (2012) Photosynthetic water splitting: Apparatus and mechanism. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Springer, Dordrecht, pp 359–414

    Chapter  Google Scholar 

  • Rögner M, Dekker JP, Boekema EJ, Witt HT (1987) Size, shape and mass of the oxygen-evolving photosystem II complex from the thermophilic cyanobacterium Synechococcus sp. FEBS Lett 219:207–211

    Article  Google Scholar 

  • Rokka A, Suorsa M, Saleem A, Battchikova N, Aro E-M (2005) Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem J 388:159–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakurai I, Hagio M, Gombos Z, Tyystjärvi T, Paakkarinen V, Aro E-M, Wada H (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiol 133:1376–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  CAS  PubMed  Google Scholar 

  • Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci U S A 106:3237–3242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi T, Inoue-Kashino N, Ozawa S, Takahashi Y, Kashino Y, Satoh K (2009) Photosystem II complex in vivo is a monomer. J Biol Chem 284:15598–15606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376

    Article  Google Scholar 

  • Tyystjärvi E, Aro E-M (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209–217

    Article  CAS  PubMed  Google Scholar 

  • Watanabe M, Iwai M, Narikawa R, Ikeuchi M (2009) Is the photosystem II complex a monomer or a dimer? Plant Cell Physiol 50:1674–1680

    Article  CAS  PubMed  Google Scholar 

  • Wu H, Cockshutt AM, McCarthy A, Campbell DA (2011) Distinctive photosystem II photoinactivation and protein dynamics in marine diatoms. Plant Physiol 156:2184–2195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu H, Roy S, Alami M, Green BR, Campbell DA (2012) Photosystem II photoinactivation, repair, and protection in marine centric diatoms. Plant Physiol 160:464–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education of Japan (No. 24370025, 26220801 to T.T., No. 17657013, 20370018, 21657013 to M.I.), by a grant from JST PRESTO to T.T., by a grant from Australian Research Council’s Discovery Projects funding scheme (project number DP12101360) to T.T., and by the Global COE program (From the Earth to ‘Earths’) to M.I.

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Authors and Affiliations

  1. Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, 464-8602, Japan

    Ryo Nagao

  2. Department of Biology, Faculty of Science, Tokyo University of Science, Kagurazaka 1-3, Shinjuku-ku, Tokyo, 162-8601, Japan

    Tatsuya Tomo & Isao Enami

  3. Precursory Research for Embryonic Science and Technology, Japan Science and Technology Agency (JST), 4-1-8 Honcho, Kawaguchi, Saitama, 332-0012, Japan

    Tatsuya Tomo

  4. Department of Biological Science, Faculty of Science, Shizuoka University, Ohya, Suruga-ku, Shizuoka, 422-8529, Japan

    Rei Narikawa

  5. Department of Life Sciences (Biology), Graduate School of Art and Sciences, University of Tokyo, Komaba 3-8-1, Meguro-ku, Tokyo, 153-8902, Japan

    Masahiko Ikeuchi

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  1. Ryo Nagao
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  2. Tatsuya Tomo
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  3. Rei Narikawa
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  4. Isao Enami
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  5. Masahiko Ikeuchi
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Correspondence to Ryo Nagao.

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Nagao, R., Tomo, T., Narikawa, R. et al. Conversion of photosystem II dimer to monomers during photoinhibition is tightly coupled with decrease in oxygen-evolving activity in the diatom Chaetoceros gracilis . Photosynth Res 130, 83–91 (2016). https://doi.org/10.1007/s11120-016-0226-1

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