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Photosynthesis Research

, Volume 137, Issue 2, pp 281–293 | Cite as

Absolute quantification of selected photosynthetic electron transfer proteins in Chlamydomonas reinhardtii in the presence and absence of oxygen

  • Denitsa Nikolova
  • Claudia Heilmann
  • Susan Hawat
  • Philipp Gäbelein
  • Michael Hippler
Original Article

Abstract

The absolute amount of plastocyanin (PC), ferredoxin-NADP+-oxidoreductase (FNR), hydrogenase (HYDA1), and ferredoxin 5 (FDX5) were quantified in aerobic and anaerobic Chlamydomonas reinhardtii whole cells using purified (recombinant) proteins as internal standards in a mass spectrometric approach. Quantified protein amounts were related to the estimated amount of PSI. The ratios of PC to FNR to HYDA1 to FDX5 in aerobic cells were determined to be 1.4:1.2:0.003:0. In anaerobic cells, the ratios changed to 1.1:1.3:0.019:0.027 (PC:FNR:HYDA1:FDX5). Employing sodium dithionite and methyl viologen as electron donors, the specific activity of hydrogenase in whole cells was calculated to be 382 ± 96.5 μmolH2 min−1 mg−1. Importantly, these data reveal an about 70-fold lower abundance of HYDA1 compared to FNR. Despite this great disproportion between both proteins, which might further enhance the competition for electrons, the alga is capable of hydrogen production under anaerobic conditions, thus pointing to an efficient channeling mechanism of electrons from FDX1 to the HYDA1.

Keywords

Plastocyanin Hydrogenase Ferredoxin-NADP+-oxidoreductase Absolute quantification Ferredoxin 5 Chlamydomonas reinhardtii 

Notes

Acknowledgements

We are grateful to Prof. Dr. Thomas Happe from the University of Bochum for providing the plasmid pJJ18. M.H. acknowledges support from the German Science Foundation (DFG, HI 739/13-1).

Funding

This study was funded by the German Science Foundation (DFG, HI 739/13-1).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Andersen B, Scheller HV, Moller BL (1992) The PSI-E subunit of photosystem I binds ferredoxin:NADP + oxidoreductase. FEBS Lett 311(2):169–173CrossRefPubMedGoogle Scholar
  2. Böhme H (1978) Quantitative determination of ferredoxin, ferredoxin-NADP + reductase and plastocyanin in spinach chloroplasts. Eur J Biochem 83:137–141CrossRefPubMedGoogle Scholar
  3. Bruska MK, Stiebritz MT, Reiher M (2011) Regioselectivity of H cluster oxidation. J Am Chem Soc 133(50):20588–20603.  https://doi.org/10.1021/ja209165r CrossRefPubMedPubMedCentralGoogle Scholar
  4. Burkey KO, Gizlice Z, Carter TE Jr (1996) Genetic variation in soybean photosynthetic electron transport capacity is related to plastocyanin concentration in the chloroplast. Photosynth Res 49(2):141–149.  https://doi.org/10.1007/BF00117664 CrossRefPubMedGoogle Scholar
  5. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25(9):1327–1333.  https://doi.org/10.1002/elps.200305844 CrossRefPubMedGoogle Scholar
  6. Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, Gatto L, Fischer B, Pratt B, Egertson J, Hoff K, Kessner D, Tasman N, Shulman N, Frewen B, Baker TA, Brusniak MY, Paulse C, Creasy D, Flashner L, Kani K, Moulding C, Seymour SL, Nuwaysir LM, Lefebvre B, Kuhlmann F, Roark J, Rainer P, Detlev S, Hemenway T, Huhmer A, Langridge J, Connolly B, Chadick T, Holly K, Eckels J, Deutsch EW, Moritz RL, Katz JE, Agus DB, MacCoss M, Tabb DL, Mallick P (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol 30(10):918–920.  https://doi.org/10.1038/nbt.2377 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Craig R, Beavis RC (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20(9):1466–1467.  https://doi.org/10.1093/bioinformatics/bth092 CrossRefPubMedGoogle Scholar
  8. Deutsch EW, Csordas A, Sun Z, Jarnuczak A, Perez-Riverol Y, Ternent T, Campbell DS, Bernal-Llinares M, Okuda S, Kawano S, Moritz RL, Carver JJ, Wang M, Ishihama Y, Bandeira N, Hermjakob H, Vizcaino JA (2017) The ProteomeXchange consortium in 2017: supporting the cultural change in proteomics public data deposition. Nucleic Acids Res 45(D1):D1100–D1106.  https://doi.org/10.1093/nar/gkw936 CrossRefPubMedGoogle Scholar
  9. Eilenberg H, Weiner I, Ben-Zvi O, Pundak C, Marmari A, Liran O, Wecker MS, Milrad Y, Yacoby I (2016) The dual effect of a ferredoxin-hydrogenase fusion protein in vivo: successful divergence of the photosynthetic electron flux towards hydrogen production and elevated oxygen tolerance. Biotechnol Biofuels 9(1):182.  https://doi.org/10.1186/s13068-016-0601-3 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Eriksson M, Moseley JL, Tottey S, Del Campo JA, Quinn J, Kim Y, Merchant S (2004) Genetic dissection of nutritional copper signaling in chlamydomonas distinguishes regulatory and target genes. Genetics 168(2):795–807.  https://doi.org/10.1534/genetics.104.030460 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Finkelmann AR, Stiebritz MT, Reiher M (2014) Activation barriers of oxygen transformation at the active site of [FeFe] hydrogenases. Inorg Chem 53(22):11890–11902.  https://doi.org/10.1021/ic501049z CrossRefPubMedGoogle Scholar
  12. Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain. J Biol Chem 276(9):6125–6132.  https://doi.org/10.1074/jbc.M008470200 CrossRefPubMedGoogle Scholar
  13. Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270(13):2750–2758CrossRefPubMedGoogle Scholar
  14. Geer LY, Markey SP, Kowalak JA, Wagner L, Xu M, Maynard DM, Yang X, Shi W, Bryant SH (2004) Open mass spectrometry search algorithm. J Proteome Res 3(5):958–964.  https://doi.org/10.1021/pr0499491 CrossRefPubMedGoogle Scholar
  15. Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 100(12):6940–6945.  https://doi.org/10.1073/pnas.0832254100 CrossRefPubMedGoogle Scholar
  16. Ghirardi ML(2015) Implementation of photobiological H2 production: the O2 sensitivity of hydrogenases. Photosynth Res 125(3):383–393.  https://doi.org/10.1007/s11120-015-0158-1 CrossRefPubMedGoogle Scholar
  17. Ghirardi ML, Togasaki RK, Seibert M (1997) Oxygen sensitivity of algal H2- production. Appl Biochem Biotechnol 63–65:141–151.  https://doi.org/10.1007/BF02920420 CrossRefPubMedGoogle Scholar
  18. Girbal L, von Abendroth G, Winkler M, Benton PM, Meynial-Salles I, Croux C, Peters JW, Happe T, Soucaille P (2005) Homologous and heterologous overexpression in Clostridium acetobutylicum and characterization of purified clostridial and algal Fe-only hydrogenases with high specific activities. Appl Environ Microbiol 71(5):2777–2781.  https://doi.org/10.1128/AEM.71.5.2777-2781.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Godaux D, Bailleul B, Berne N, Cardol P (2015) Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and proton-gradient regulation-like1-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol 168(2):648–658.  https://doi.org/10.1104/pp.15.00105 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Graan T, Ort DR (1984) Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts. J Biol Chem 259(22):14003–14010PubMedGoogle Scholar
  21. Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269(3):1022–1032CrossRefPubMedGoogle Scholar
  22. Happe T, Naber JD (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214(2):475–481CrossRefPubMedGoogle Scholar
  23. Harris EH (1989) The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Academic Press, San DiegoGoogle Scholar
  24. Havlis J, Shevchenko A (2004) Absolute quantification of proteins in solutions and in polyacrylamide gels by mass spectrometry. Anal Chem 76(11):3029–3036.  https://doi.org/10.1021/ac035286f CrossRefPubMedGoogle Scholar
  25. Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807(8):919–926.  https://doi.org/10.1016/j.bbabio.2011.02.010 CrossRefPubMedGoogle Scholar
  26. Hippler M, Drepper F, Farah J, Rochaix JD (1997) Fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii requires PsaF. Biochemistry 36(21):6343–6349.  https://doi.org/10.1021/bi970082c CrossRefPubMedGoogle Scholar
  27. Hippler M, Klein J, Fink A, Allinger T, Hoerth P (2001) Towards functional proteomics of membrane protein complexes: analysis of thylakoid membranes from Chlamydomonas reinhardtii. Plant J 28(5):595–606CrossRefPubMedGoogle Scholar
  28. Hong G, Pachter R (2012) Inhibition of biocatalysis in [Fe-Fe] hydrogenase by oxygen: molecular dynamics and density functional theory calculations. ACS Chem Biol 7(7):1268–1275.  https://doi.org/10.1021/cb3001149 CrossRefPubMedGoogle Scholar
  29. Hulsker R, Mery A, Thomassen EA, Ranieri A, Sola M, Verbeet MP, Kohzuma T, Ubbink M (2007) Protonation of a histidine copper ligand in fern plastocyanin. J Am Chem Soc 129(14):4423–4429.  https://doi.org/10.1021/ja0690464 CrossRefPubMedGoogle Scholar
  30. Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464(7292):1210–1213.  https://doi.org/10.1038/nature08885 CrossRefPubMedGoogle Scholar
  31. Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583(2):325–329.  https://doi.org/10.1016/j.febslet.2008.12.018 CrossRefPubMedGoogle Scholar
  32. Joliot P, Delosme R (1974) Flash-induced 519 nm absorption change in green algae. Biochim Biophys Acta 357(2):267–284CrossRefPubMedGoogle Scholar
  33. Kamp C, Silakov A, Winkler M, Reijerse EJ, Lubitz W, Happe T (2008) Isolation and first EPR characterization of the [FeFe]-hydrogenases from green algae. Biochim Biophys Acta 1777(5):410–416.  https://doi.org/10.1016/j.bbabio.2008.02.002 CrossRefPubMedGoogle Scholar
  34. Katoh S (1977) Encyclopedia of plant physiology,” new series. In: Trebst A, Avron M (eds) Photosynthesis I, Vol. 5, Springer, Berlin, pp 247–252CrossRefGoogle Scholar
  35. Kirkpatrick DS, Gerber SA, Gygi SP (2005) The absolute quantification strategy: a general procedure for the quantification of proteins and post-translational modifications. Methods 35(3):265–273.  https://doi.org/10.1016/j.ymeth.2004.08.018 CrossRefPubMedGoogle Scholar
  36. Kubas A, Orain C, De Sancho D, Saujet L, Sensi M, Gauquelin C, Meynial-Salles I, Soucaille P, Bottin H, Baffert C, Fourmond V, Best RB, Blumberger J, Leger C (2017) Mechanism of O2 diffusion and reduction in FeFe hydrogenases. Nat Chem 9(1):88–95.  https://doi.org/10.1038/nchem.2592 PubMedGoogle Scholar
  37. Kuhlgert S, Drepper F, Fufezan C, Sommer F, Hippler M (2012) Residues PsaB Asp612 and PsaB Glu613 of photosystem I confer pH-dependent binding of plastocyanin and cytochrome c(6). Biochemistry 51(37):7297–7303.  https://doi.org/10.1021/bi300898j CrossRefPubMedGoogle Scholar
  38. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685CrossRefPubMedGoogle Scholar
  39. Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryot Cell 9(11):1747–1754.  https://doi.org/10.1128/EC.00127-10 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lambertz C, Leidel N, Havelius KG, Noth J, Chernev P, Winkler M, Happe T, Haumann M (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J Biol Chem 286(47):40614–40623.  https://doi.org/10.1074/jbc.M111.283648 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lien S, Pietro AS (1979) Interaction of plastocyanin and P700 in PSI reaction centre particles from Chlamydomonas reinhardtii and spinach. Arch Biochem Biophys 194(No.1):128–137CrossRefPubMedGoogle Scholar
  42. Liran O, Semyatich R, Milrad Y, Eilenberg H, Weiner I, Yacoby I (2016) Microoxic Niches within the thylakoid stroma of air-grown Chlamydomonas reinhardtii protect [FeFe]-hydrogenase and support hydrogen production under fully aerobic environment. Plant Physiol 172(1):264–271.  https://doi.org/10.1104/pp.16.01063 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127(3):740–748CrossRefPubMedPubMedCentralGoogle Scholar
  44. Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122(1):127–136CrossRefPubMedPubMedCentralGoogle Scholar
  45. Meuser JE, D’Adamo S, Jinkerson RE, Mus F, Yang W, Ghirardi ML, Seibert M, Grossman AR, Posewitz MC (2012) Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H(2) production. Biochem Biophys Res Commun 417(2):704–709.  https://doi.org/10.1016/j.bbrc.2011.12.002 CrossRefPubMedGoogle Scholar
  46. Mosebach L, Heilmann C, Mutoh R, Gabelein P, Steinbeck J, Happe T, Ikegami T, Hanke G, Kurisu G, Hippler M (2017) Association of ferredoxin:NADP + oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii. Photosynth Res.  https://doi.org/10.1007/s11120-017-0408-5 PubMedPubMedCentralGoogle Scholar
  47. Mulder DW, Ortillo DO, Gardenghi DJ, Naumov AV, Ruebush SS, Szilagyi RK, Huynh B, Broderick JB, Peters JW (2009) Activation of HydA(DeltaEFG) requires a preformed [4Fe-4S] cluster. Biochemistry 48(26):6240–6248.  https://doi.org/10.1021/bi9000563 CrossRefPubMedGoogle Scholar
  48. Mulder DW, Boyd ES, Sarma R, Lange RK, Endrizzi JA, Broderick JB, Peters JW (2010) Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(DeltaEFG). Nature 465(7295):248–251.  https://doi.org/10.1038/nature08993 CrossRefPubMedGoogle Scholar
  49. Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H(2) photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708(3):322–332.  https://doi.org/10.1016/j.bbabio.2005.05.003 CrossRefPubMedGoogle Scholar
  50. Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282(35):25475–25486.  https://doi.org/10.1074/jbc.M701415200 CrossRefPubMedGoogle Scholar
  51. Nawrocki WJ, Santabarbara S, Mosebach L, Wollman FA, Rappaport F (2016) State transitions redistribute rather than dissipate energy between the two photosystems in Chlamydomonas. Nat Plants 2:16031.  https://doi.org/10.1038/nplants.2016.31 CrossRefPubMedGoogle Scholar
  52. Onda Y, Matsumura T, Kimata-Ariga Y, Sakakibara H, Sugiyama T, Hase T (2000) Differential interaction of maize root ferredoxin:NADP(+) oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins. Plant Physiol 123(3):1037–1046CrossRefPubMedPubMedCentralGoogle Scholar
  53. Ong SE, Mann M (2005) Mass spectrometry-based proteomics turns quantitative. Nat Chem Biol 1(5):252–262.  https://doi.org/10.1038/nchembio736 CrossRefPubMedGoogle Scholar
  54. Peden EA, Boehm M, Mulder DW, Davis R, Old WM, King PW, Ghirardi ML, Dubini A (2013) Identification of global ferredoxin interaction networks in Chlamydomonas reinhardtii. J Biol Chem 288(49):35192–35209.  https://doi.org/10.1074/jbc.M113.483727 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282(5395):1853–1858CrossRefPubMedGoogle Scholar
  56. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975(3):384–394.  https://doi.org/10.1016/S0005-2728(89)80347-0 CrossRefGoogle Scholar
  57. Quinn JM, Barraco P, Eriksson M, Merchant S (2000) Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 275(9):6080–6089CrossRefPubMedGoogle Scholar
  58. Quinn JM, Eriksson M, Moseley JL, Merchant S (2002) Oxygen deficiency responsive gene expression in Chlamydomonas reinhardtii through a copper-sensing signal transduction pathway. Plant Physiol 128(2):463–471.  https://doi.org/10.1104/pp.010694 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Roessler PG, Lien S (1984a) Activation and de novo synthesis of hydrogenase in chlamydomonas. Plant Physiol 76(4):1086–1089CrossRefPubMedPubMedCentralGoogle Scholar
  60. Roessler PG, Lien S (1984b) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75(3):705–709CrossRefPubMedPubMedCentralGoogle Scholar
  61. Rupprecht J, Hankamer B, Mussgnug JH, Ananyev G, Dismukes C, Kruse O (2006) Perspectives and advances of biological H2 production in microorganisms. Appl Microbiol Biotechnol 72(3):442–449.  https://doi.org/10.1007/s00253-006-0528-x CrossRefPubMedGoogle Scholar
  62. Sawyer A, Winkler M (2017) Evolution of Chlamydomonas reinhardtii ferredoxins and their interactions with [FeFe]-hydrogenases. Photosynth Res.  https://doi.org/10.1007/s11120-017-0409-4 PubMedGoogle Scholar
  63. Sawyer A, Bai Y, Lu Y, Hemschemeier A, Happe T (2017) Compartmentalisation of [FeFe]-hydrogenase maturation in Chlamydomonas reinhardtii. Plant J 90(6):1134–1143.  https://doi.org/10.1111/tpj.13535 CrossRefPubMedGoogle Scholar
  64. Schottler MA, Kirchhoff H, Weis E (2004) The role of plastocyanin in the adjustment of the photosynthetic electron transport to the carbon metabolism in tobacco. Plant Physiol 136(4):4265–4274.  https://doi.org/10.1104/pp.104.052324 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Steinbeck J, Nikolova D, Weingarten R, Johnson X, Richaud P, Peltier G, Hermann M, Magneschi L, Hippler M (2015) Deletion of proton gradient regulation 5 (PGR5) and PGR5-Like 1 (PGRL1) proteins promote sustainable light-driven hydrogen production in Chlamydomonas reinhardtii due to increased PSII activity under sulfur deprivation. Front Plant Sci 6:892.  https://doi.org/10.3389/fpls.2015.00892 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Proc Natl Acad Sci USA 106(41):17331–17336.  https://doi.org/10.1073/pnas.0905343106 CrossRefPubMedGoogle Scholar
  67. Swanson KD, Ratzloff MW, Mulder DW, Artz JH, Ghose S, Hoffman A, White S, Zadvornyy OA, Broderick JB, Bothner B, King PW, Peters JW (2015) [FeFe]-hydrogenase oxygen inactivation is initiated at the H cluster 2Fe subcluster. J Am Chem Soc 137(5):1809–1816.  https://doi.org/10.1021/ja510169s CrossRefPubMedGoogle Scholar
  68. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9(7):1514–1532.  https://doi.org/10.1074/mcp.M900421-MCP200 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284(38):25867–25878.  https://doi.org/10.1074/jbc.M109.023622 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Vizcaino JA, Csordas A, Del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, Xu QW, Wang R, Hermjakob H (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44(22):11033.  https://doi.org/10.1093/nar/gkw880 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Volgusheva A, Styring S, Mamedov F (2013) Increased photosystem II stability promotes H2 production in sulfur-deprived Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110(18):7223–7228.  https://doi.org/10.1073/pnas.1220645110 CrossRefPubMedGoogle Scholar
  72. Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae. J Biol Chem 284(52):36620–36627.  https://doi.org/10.1074/jbc.M109.053496 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang S (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin:NADP+-oxidoreductase (FNR) enzymes in vitro. Proc Natl Acad Sci USA 108(23):9396–9401.  https://doi.org/10.1073/pnas.1103659108 CrossRefPubMedGoogle Scholar
  74. Yacoby I, Tegler LT, Pochekailov S, Zhang S, King PW, Riggs PD (2012) Optimized expression and purification for high-activity preparations of Algal [FeFe]-Hydrogenase. PLoS ONE 7(4):e35886CrossRefPubMedPubMedCentralGoogle Scholar
  75. Yang W, Wittkopp TM, Li X, Warakanont J, Dubini A, Catalanotti C, Kim RG, Nowack EC, Mackinder LC, Aksoy M, Page MD, D’Adamo S, Saroussi S, Heinnickel M, Johnson X, Richaud P, Alric J, Boehm M, Jonikas MC, Benning C, Merchant SS, Posewitz MC, Grossman AR (2015) Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. Proc Natl Acad Sci USA 112(48):14978–14983.  https://doi.org/10.1073/pnas.1515240112 CrossRefPubMedGoogle Scholar
  76. Zalutskaya Z, Minaeva E, Filina V, Ostroukhova M, Ermilova E (2017) Regulation of sulfur deprivation-induced expression of the ferredoxin-encoding FDX5 gene Chlamydomonas reinhardtii in aerobic conditions. Plant Physiol Biochem 123:18–23.  https://doi.org/10.1016/j.plaphy.2017.11.024 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Institut für Biologie und Biotechnologie der PflanzenWestfälische Wilhelms-Universität MünsterMünsterGermany

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