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The photosynthetic cytochrome c 550 from the diatom Phaeodactylum tricornutum

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Abstract

The photosynthetic cytochrome c 550 from the marine diatom Phaeodactylum tricornutum has been purified and characterized. Cytochrome c 550 is mostly obtained from the soluble cell extract in relatively large amounts. In addition, the protein appeared to be truncated in the last hydrophobic residues of the C-terminus, both in the soluble cytochrome c 550 and in the protein extracted from the membrane fraction, as deduced by mass spectrometry analysis and the comparison with the gene sequence. Interestingly, it has been described that the C-terminus of cytochrome c 550 forms a hydrophobic finger involved in the interaction with photosystem II in cyanobacteria. Cytochrome c 550 was almost absent in solubilized photosystem II complex samples, in contrast with the PsbO and Psb31 extrinsic subunits, thus suggesting a lower affinity of cytochrome c 550 for the photosystem II complex. Under iron-limiting conditions the amount of cytochrome c 550 decreases up to about 45% as compared to iron-replete cells, pointing to an iron-regulated synthesis. Oxidized cytochrome c 550 has been characterized using continuous wave EPR and pulse techniques, including HYSCORE, and the obtained results have been interpreted in terms of the electrostatic charge distribution in the surroundings of the heme centre.

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Abbreviations

ß-DM:

ß-dodecyl-maltoside

Cc550 :

Cytochrome c 550

Cc6 :

Cytochrome c 6

CW:

Continuous wave

EPR:

Electron paramagnetic resonance

HYSCORE:

Hyperfine sublevel correlation spectroscopy

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

PSII:

Photosystem II

References

  • Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, Wang F, Zou H, Enami I, Miyano M, Shen J-R (2016) Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem 291:5676–5687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alam J, Sprinkle MA, Hermodson MA, Krogmann DW (1984) Characterization of cytochrome c-550 from cyanobacteria. Biochim Biophys Acta 766:317–321

    Article  CAS  Google Scholar 

  • Allen AE, Laroche J, Maheswari U, Lommer M, Schauer N, Lopez PJ, Finazzi G, Fernie AR, Bowler C (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci USA 105:10438–10443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alonso PJ, Martínez JI (2015) Magnetic properties of a Kramers doublet. An univocal bridge between experimental results and theoretical predictions. J Magn Res 255:1–14

    Article  CAS  Google Scholar 

  • Alonso PJ, Martínez JI, García-Rubio I (2007) The study of the ground state Kramers doublet of low-spin heminic system revisited. A comprehensive description of the EPR and Mössbauer spectra. Coord Chem Rev 152:12–24

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aro EM, 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 

  • Bernal-Bayard P, Molina-Heredia FP, Hervás M, Navarro JA (2013) Photosystem I reduction in diatoms: as complex as the green lineage systems but less efficient. Biochemistry 52:8687–8695

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Allen AE, Badger JH et al (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

    Article  CAS  PubMed  Google Scholar 

  • Bowler C, Vardi A, Allen AE (2010) Oceanographic and biogeochemical insights from diatom genomes. Ann Rev Mar Sci 2:333–365

    Article  PubMed  Google Scholar 

  • Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ (2012) The extrinsic proteins of Photosystem II. Biochim Biophys Acta 1817:121–142

    Article  CAS  PubMed  Google Scholar 

  • Bumba L, Havelková-Dousová H, Husák M, Vácha F (2004) Structural characterization of photosystem II complex from red alga Porphyridium cruentum retaining extrinsic subunits of the oxygen-evolving complex. Eur J Biochem 271:2967–2975

    Article  CAS  PubMed  Google Scholar 

  • Crimmins DL, Mische SM, Denslow ND (2005) Chemical cleavage of proteins in solution. Curr Protoc Protein Sci Supp. 41:11.4.1–11.4.11

    Article  Google Scholar 

  • Durán RV, Hervás M, De la Rosa MA, Navarro JA (2005) In vivo photosystem I reduction in thermophilic and mesophilic cyanobacteria: The thermal resistance of the process is limited by factors other than the unfolding of the partners. Biochem Biophys Res Commun 334:170–175

    Article  PubMed  Google Scholar 

  • Enami I, Murayama H, Ohta H, Kamo M, Nakazato K, Shen J-R (1995) Isolation and characterizaton of a photosystem II complex from a red alga Cyanidium caldarium: association of cytochrome c-550 and a 12 kDa protein with the complex. Biochim Biophys Acta 1232:208–216

    Article  PubMed  Google Scholar 

  • Enami I, Kikuchi S, Fukuda T, Ohta H, Shen J-R (1998) Binding and functional properties of four extrinsic proteins of photosystem II from a red alga, Cyanidium caldarium, as studied by release-reconstitution experiments. Biochemistry 37:2787–2793

    Article  CAS  PubMed  Google Scholar 

  • Enami I, Iwai M, Akiyama A, Suzuki T, Okumura A, Katoh T, Tada O, Ohta H, Shen J-R (2003) Comparison of binding and functional properties of two extrinsic components, Cyt c550 and a 12 kDa protein, in cyanobacterial PSII with those in red algal PSII. Plant Cell Physiol 44:820–827

    Article  CAS  PubMed  Google Scholar 

  • Enami I, Okumura A, Nagao R, Suzuki T, Iwai M, Shen J-R (2008) Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth Res 98:349–363

    Article  CAS  PubMed  Google Scholar 

  • Evans PK, Krogmann DW (1983) Three c-type cytochromes from the red alga Porphyridium cruentum. Arch Biochem Biophys 227:494–510

    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 

  • Frazão C, Enguita FJ, Coelho R, Sheldrick GM, Navarro JA, Hervás M, De la Rosa MA, Carrondo MA (2001) Crystal structure of low-potential cytochrome c 549 from Synechocystis sp. PCC 6803 at 1.21 Å resolution. J Biol Inorg Chem 6:324–332

    Article  PubMed  Google Scholar 

  • García-Rubio I, Martínez JI, Picorel R, Yruela I, Alonso PJ (2003) HYSCORE spectroscopy in the cytochrome b(559) of the photosystem II reaction center. J Am Chem Soc 125:15846–15854

    Article  PubMed  Google Scholar 

  • Goldman JC, McCarthy JJ (1978) Steady state growth and ammonium uptake of a fast-growing marine diatom 1. Limnol Oceanogr 23:695–703

    Article  CAS  Google Scholar 

  • Griffith JS (1957) Theory of electron resonance in ferrihaemoglobin azide. Nature 180:30–31

    Article  CAS  PubMed  Google Scholar 

  • Grouneva I, Rokka A, Aro E-M (2011) The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res 10:5338–5353

    Article  CAS  PubMed  Google Scholar 

  • Grouneva I, Gollan PJ, Kangasjärvi S, Suorsa M, Tikkanen M, Aro E-M (2013) Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms. Planta 237:399–412

    Article  CAS  PubMed  Google Scholar 

  • Guerrero F, Sedoud A, Kirilovsky D, Rutherford AW, Ortega JM, Roncel M (2011) A high redox potential form of cytochrome c 550 in Photosystem II from Thermosynechococcus elongatus. J Biol Chem 286:5985–5994

    Article  CAS  PubMed  Google Scholar 

  • Guerrero F, Zurita JL, Roncel M, Kirilovsky D, Ortega JM (2014) The role of the high potential form of the cytochrome b 559: study of Thermosynechococcus elongatus mutants. Biochim Biophys Acta 1837:908–919

    Article  CAS  PubMed  Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18:2714–2723

    Article  CAS  PubMed  Google Scholar 

  • Haehnel W, Ratajczak R, Robenek H (1989) Lateral distribution and diffusion of plastocyanin in chloroplast thylakoids. J Cell Biol 108:1397–1405

    Article  CAS  PubMed  Google Scholar 

  • Ifuku K, Noguchi T (2016) Structural coupling of extrinsic proteins with the oxygen-evolving center in photosystem II. Front Plant Sci 7:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Ioanitescu AI, Van Doorslaer S, Dewilde S, Endeward B, Moens L (2007) Probing the heme-pocket structure of the paramagnetic forms of cytoglobin and a distal histidine mutant using electron paramagnetic resonance. Mol Phys 105:2073–2086

    Article  CAS  Google Scholar 

  • Jeffrey S, Humphrey G (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194

    Article  CAS  Google Scholar 

  • Kang C, Chitnis RP, Smith S, Krogmann DW (1994) Cloning and sequence analysis of the gene encoding the low potential cytochrome c of Synechocystis PCC 6803. FEBS Lett 344:5–9

    Article  CAS  PubMed  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 

  • Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nat Protoc 4:363–371

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA, Krogmann DW (1998) Photosynthetic cytochromes c in cyanobacteria, algae and plants. Annu Rev Plant Physiol Plant Mol Biol 49:397–425

    Article  CAS  PubMed  Google Scholar 

  • Kerfeld CA, Sawaya MR, Bottin H, Tran KT, Sugiura M, Cascio D, Desbois A, Yeates TO, Kirilovsky D, Boussac A (2003) Structural and EPR characterization of the soluble form of cytochrome c-550 and of the psbV2 gene product from the cyanobacterium Thermosynechococcus elongatus. Plant Cell Physiol 44:697–706

    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 

  • Kienzel PF, Peschek GA (1983) Cytochrome c-549: an endogenous cofactor of cyclic photophosphorylation in the cyanobacterium Anacystis nidulans. FEBS Lett 162:76–80

    Article  Google Scholar 

  • Kirilovsky D, Roncel M, Boussac A, Wilson A, Zurita JL, Ducruet JM, Bottin H, Sugiura M, Ortega JM, Rutherford AW (2004) Cytochrome c 550 in the cyanobacterium Thermosynechococcus elongatus: study of redox mutants. J Biol Chem 279:52869–52880

    Article  CAS  PubMed  Google Scholar 

  • Kooistra WHCF, Gersonde R, Medlin LK, Mann DG. (2007) The origin and evolution of the diatoms: their adaptation to a planktonic existence. In: Falkowski PG, Knoll AH (eds) Evolution of primary producers in the sea, Academic Press Inc., Oxford pp. 207–249

    Chapter  Google Scholar 

  • Krogmann DW (1991) The low-potential cytochrome c of cyanobacteria and algae. Biochim Biophys Acta 1058:35–37

    Article  CAS  PubMed  Google Scholar 

  • Lavaud J, Six C, Campbell DA (2016) Photosystem II repair in marine diatoms with contrasting photophysiologies. Photosynth Res 127:189–199

    Article  CAS  PubMed  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Fábregas J, Díaz-Moreno I, González-Arzola K, Janocha S, Navarro JA, Hervás M, Bernhardt R, Velázquez-Campoy A, Díaz-Quintana A, De la Rosa MA (2014) Structural and functional analysis of novel human cytochrome c targets in apoptosis. Mol Cell Proteomics 13:1439–1456

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinson TA, Ikeuchi M, Plumley FG (1998) Oxygen-evolving diatom thylakoid membranes. Biochim Biophys Acta 1409:72–86

    Article  CAS  PubMed  Google Scholar 

  • McLachlan J (1964) Some considerations of the growth of marine algae in artificial media. Can J Microbiol 10:769–782

    Article  CAS  PubMed  Google Scholar 

  • Molina-Heredia FP, Hervás M, Navarro JA, De la Rosa MA (1998) Cloning and correct expression in Escherichia coli of the petE and petJ genes respectively encoding plastocyanin and cytochrome c 6 from the cyanobacterium Anabaena sp. PCC 7119. Biochem Biophys Res Commun 243:302–306

    Article  CAS  PubMed  Google Scholar 

  • Moore JK, Doney SC, Glover DM, Fung IY (2002) Iron cycling and nutrient-limitation patterns in surface waters of the world ocean. Deep Sea Res II(49):463–507

    Google Scholar 

  • Morand LZ, Cheng RH, Krogmann DW (1994) Soluble electron transfer catalysts of cyanobacteria. In: Bryant DA (ed) The molecular biology of cyanobacteria. Kluwer, Dordrecht, pp 381–407

    Chapter  Google Scholar 

  • Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:1–13

    Article  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

  • 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

  • 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, Tomo T, Narikawa R, Enami I, Ikeuchi M (2013) 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, Tomo T, Noguchi E (2015) Effects of extrinsic proteins on the protein conformation of the oxygen-evolving center in cyanobacterial photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 54:2022–2031

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Tomo T, Narikawa R, Enami I, Ikeuchi M (2016) 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

    Article  CAS  PubMed  Google Scholar 

  • Navarro JA, Hervás M, De la Rosa MA (2011) Purification of plastocyanin and cytochrome c6 from plants, green algae and cyanobacteria. In: Carpentier R (ed) Photosynthesis protocols, vol 684. Humana Press, Totowa, pp 79–94

  • Navarro JA, Hervás M, De la Cerda B, De la Rosa MA (1995) Purification and physicochemical properties of the low potential cytochrome c549 from the cyanobacterium Synechocystis sp. PCC 6803. Arch Biochem Biophys 3186:46–52

    Article  Google Scholar 

  • Nunn BL, Faux JF, Hippmann AA, Maldonado MT, Harvey HR, Goodlett DR, Boyd PW, Strzepek RF (2013) Diatom proteomics reveals unique acclimation strategies to mitigate Fe limitation. PLoS ONE 8: e75653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okumura A, Nagao R, Suzuki T, Yamagoe S, Iwai M, Nakazato K, Enami I (2008) A novel protein in Photosystem II of a diatom Chaetoceros gracilis is one of the extrinsic proteins located on lumenal side and directly associates with PSII core components. Biochim Biophys Acta 1777:1545–1551

    Article  CAS  PubMed  Google Scholar 

  • Peisach J, Blumberg WE, Adler A (1973) Electron paramagnetic resonance studies of iron porphin and chlorin systems. Ann NY Acad Sci 206:310–327

    Article  CAS  PubMed  Google Scholar 

  • Quinn R, Valentine JS, Byrn MP, Strouse CE (1987) Electronic-structure of low-spin ferric porphyrins: A single-crystal EPR and structural investigation of the influence of axial ligand orientation and the effects of pseudo-Jahn–Teller distortion. J Am Chem Soc 109:3301–3308

    Article  CAS  Google Scholar 

  • Roncel M, Boussac A, Zurita JL, Bottin H, Sugiura M, Kirilovsky D, Ortega JM (2003) Redox properties of the photosystem II cytochromes b 559 and c 550 in the cyanobacterium Thermosynechococcus elongatus. J Biol Inorg Chem 8:206–216

    Article  CAS  PubMed  Google Scholar 

  • Roncel M, Kirilovsky D, Guerrero F, Serrano A, Ortega JM (2012) Photosynthetic cytochrome c550. Biochim Biophys Acta 1817:1152–1163

    Article  CAS  PubMed  Google Scholar 

  • Roncel M, González-Rodríguez AA, Naranjo B, Bernal-Bayard P, Lindahl AM, Hervás M, Navarro JA, Ortega JM (2016) Iron deficiency induces a partial inhibition of the photosynthetic electron transport and a high sensitivity to light in the diatom Phaeodactylum tricornutum. Front Plant Sci 7:1050

    Article  PubMed  PubMed Central  Google Scholar 

  • Sawaya MR, Krogmann DW, Serag A, Ho KK, Yeates TO, Kerfeld CA (2001) Structures of cytochrome c-549 and cytochrome c6 from the cyanobacterium Arthrospira maxima. Biochemistry 40:9215–9225

    Article  CAS  PubMed  Google Scholar 

  • Schweiger A, Jeschke G. (2001) Principles of pulse electron paramagnetic resonance. Oxford University Press, Oxford

  • Sechi S, Chait BT (1998) Modification of cysteine residues by alkylation. A tool in peptide mapping and protein identification. Anal Chem 70:5150–5158

    Article  CAS  PubMed  Google Scholar 

  • Shen J-R (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48

    Article  CAS  PubMed  Google Scholar 

  • Shen J-R, Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. Biochemistry 32:1825–1832

    Article  CAS  PubMed  Google Scholar 

  • Shen J-R, Qian M, Inoue Y, Burnap RL (1998) Functional characterization of Synechocystis sp. 6803 ∆psbU and ∆psbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37:1551–1558

    Article  CAS  PubMed  Google Scholar 

  • Shimazaki K, Takamiya K, Nishimura M (1978) Studies on electron transfer systems in the marine diatom Phaeodactylum tricornutum. I. Isolation and characterization of cytochromes. J Biochem 83:1631–1638

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Lai T-L, Sugiura M, Shen J-R, Boussac A (2013) Crystal structure at 1.5 Å resolution of the PsbV2 cytochrome from the cyanobacterium Thermosynechococcus elongatus. FEBS Lett 587:3267–3272

    Article  CAS  PubMed  Google Scholar 

  • Takaoka T, Sakashita N, Saito K, Ishikita H (2016) pKa of a proton-conducting water chain in photosystem II. ‎J Phys Chem Lett 7:1925–1932

    Article  CAS  PubMed  Google Scholar 

  • Taylor CPS (1977) The EPR of low spin heme complexes. Relation of the t2g hole model to the directional properties of the g tensor, and a new method for calculating the ligand field parameters. Biochim Biophys Acta 491:137–149

    Article  CAS  PubMed  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 

  • Van Doorslaer S, Tilleman L, Verrept B, Dewilde S (2012) Marked difference in the electronic structure of cyanide-ligated ferric protoglobins and myoglobin due to heme ruffling. Inorg Chem 51:8834–8841

    Article  PubMed  Google Scholar 

  • Vogt L, Vinyard DJ, Khan S, Brudvig GW (2015) Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks. Curr Opin Chem Biol 25:152–158

    Article  CAS  PubMed  Google Scholar 

  • Vrettos JS, Reifler MJ, Kievit O, Lakshmi KV, Lakshmi JC, de Paula JC, Brudvig GW (2001) Factors that determine the unusually low reduction potential of cytochrome c550 in cyanobacterial photosystem II. J Biol Inorg Chem 6:708–716

    Article  CAS  PubMed  Google Scholar 

  • Walker FA, Huynh BH, Scheidt WR, Osvath RS (1986) Models of the cytochromes b. Effect of axial ligand plane orientation on the EPR and Mössbauer spectra of low-spin ferrihemes. J Am Chem Soc 108:5288–5297

    Article  CAS  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 

  • Yruela I, García-Rubio I, Roncel M, Martínez JI, Ramiro MV, Ortega JM, Alonso PJ, Picorel R (2003) Detergent effect on cytochrome b 559 electron paramagnetic resonance signals in the photosystem II reaction centre. Photochem Photobiol Sci 2:437–442

    Article  CAS  PubMed  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of oxygen evolving Photosystem II from Synechococcus elongatus a 3.8 Å resolution. Nature 409:739–743

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Rocío Rodríguez (Proteomic Service, IBVF) for technical assistance, and Prof. Tatsuya Tomo (Tokyo University of Science, Japan) for the Psb31 antibodies.

Funding

This work was supported by the Spanish Ministry of Economy and Competitiveness (BIO2012-35271, BIO2015-64169-P, MAT2011-23861 and CTQ2015-64486-R) the Andalusian Government (PAIDI BIO-022) and the Aragón Government (Grupo consolidado B-18). All these grants were partially financed by the EU FEDER Program.

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Bernal-Bayard, P., Puerto-Galán, L., Yruela, I. et al. The photosynthetic cytochrome c 550 from the diatom Phaeodactylum tricornutum . Photosynth Res 133, 273–287 (2017). https://doi.org/10.1007/s11120-016-0327-x

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