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Auxiliary electron transport pathways in chloroplasts of microalgae

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Abstract

Microalgae are photosynthetic organisms which cover an extraordinary phylogenic diversity and have colonized extremely diverse habitats. Adaptation to contrasted environments in terms of light and nutrient’s availabilities has been possible through a high flexibility of the photosynthetic machinery. Indeed, optimal functioning of photosynthesis in changing environments requires a fine tuning between the conversion of light energy by photosystems and its use by metabolic reaction, a particularly important parameter being the balance between phosphorylating (ATP) and reducing (NADPH) power supplies. In addition to the main route of electrons operating during oxygenic photosynthesis, called linear electron flow or Z scheme, auxiliary routes of electron transfer in interaction with the main pathway have been described. These reactions which include non-photochemical reduction of intersystem electron carriers, cyclic electron flow around PSI, oxidation by molecular O2 of the PQ pool or of the PSI electron acceptors, participate in the flexibility of photosynthesis by avoiding over-reduction of electron carriers and modulating the NADPH/ATP ratio depending on the metabolic demand. Forward or reverse genetic approaches performed in model organisms such as Arabidopsis thaliana for higher plants, Chlamydomonas reinhardtii for green algae and Synechocystis for cyanobacteria allowed identifying molecular components involved in these auxiliary electron transport pathways, including Ndh-1, Ndh-2, PGR5, PGRL1, PTOX and flavodiiron proteins. In this article, we discuss the diversity of auxiliary routes of electron transport in microalgae, with particular focus in the presence of these components in the microalgal genomes recently sequenced. We discuss how these auxiliary mechanisms of electron transport may have contributed to the adaptation of microalgal photosynthesis to diverse and changing environments.

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Abbreviations

cyt:

Cytochrome

Flv:

Flavodiiron

FNR:

Ferredoxin NADPH oxidoreductase, Ndh-1, type I NDH complex

Ndh-2:

Type II NAD(P)H dehydrogenase

PQ:

Plastoquinone

PTOX:

Plastid terminal oxidase

PS:

Photosystem

References

  • 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  PubMed  Google Scholar 

  • Arnon DI, Chain RK (1975) Regulation of ferredoxin-catalyzed photosynthetic phosphorylations. Proc Natl Acad Sci USA 72:4961–4965

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Atteia A, van Lis R, van Hellemond JJ, Tielens AGM, Martin W, Henze K (2004) Identification of prokaryotic homologues indicates an endosymbiotic origin for the alternative oxidases of mitochondria (AOX) and chloroplasts (PTOX). Gene 330:143–148

    Article  PubMed  CAS  Google Scholar 

  • Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Phil Trans R Soc Lond B 355:1433–1445

    Article  CAS  Google Scholar 

  • Baniulis D, Yamashita E, Zhang H, Hasan SS, Cramer WA (2008) Structure-function of the cytochrome b 6 f complex. Photochem Photobiol 84:1349–1358

    Article  PubMed  CAS  Google Scholar 

  • Bennoun P (1982) Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci USA 79:4352–4356

    Article  PubMed  CAS  Google Scholar 

  • Cardol P, Bailleul B, Rappaport F, Derelle E, Beal D, Breyton C, Bailey S, Wollman FA, Grossman A, Moreau H, Finazzi G (2008) An original adaptation of photosynthesis in the marine green alga Ostreococcus. Proc Natl Acad Sci USA 105:7881–7886

    Article  PubMed  Google Scholar 

  • Cardol P, Alric J, Girard-Bascou J, Franck F, Wollman FA, Finazzi G (2009) Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc Natl Acad Sci USA 106:15979–15984

    Article  PubMed  Google Scholar 

  • Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene immutans cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68

    Article  PubMed  CAS  Google Scholar 

  • Cournac L, Redding K, Ravenel J, Rumeau D, Josse E-M, Kuntz M, Peltier G (2000) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256–17262

    Article  PubMed  CAS  Google Scholar 

  • Cramer WA, Zhang HM, Yan JS, Kurisu G, Smith JL (2006) Transmembrane traffic in the cytochrome b 6 f complex. Annu Rev Biochem 75:769–790

    Article  PubMed  CAS  Google Scholar 

  • DalCorso G, Pesaresi P, Masiero S, Aseeva E, Nemann DS, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285

    Article  PubMed  CAS  Google Scholar 

  • de Cambiaire JC, Otis C, Lemieux C, Turmel M (2006) The complete chloroplast genome sequence of the chlorophycean green alga Scenedesmus obliquus reveals a compact gene organization and a biased distribution of genes on the two DNA strands. BMC Evol Biol 6:37

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J Biol Chem 284:4148–4157

    Article  PubMed  CAS  Google Scholar 

  • Dubini A, Mus F, Seibert M, Grossman AR, Posewitz MC (2009) Flexibility in anaerobic metabolism as revealed in a mutant of Chlamydomonas reinhardtii lacking hydrogenase activity. J Biol Chem 284:7201–7213

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1989) PHYLIP––phylogeny inference package (version 3.2). Cladistics 5:164–166

    Google Scholar 

  • Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129

    Article  PubMed  CAS  Google Scholar 

  • 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 276:6125–6132

    Article  PubMed  CAS  Google Scholar 

  • Fouchard S, Hemschemeier A, Caruana A, Pruvost J, Legrand J, Happe T, Peltier G, Cournac L (2005) Investigations on autotrophic and mixotrophic hydrogen photoproduction in sulphur-deprived Chlamydomonas cells. Appl Environ Microbiol 71:6199–6205

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  • Ghirardi ML, Posewitz MC, Maness PC, Dubini A, Yu JP, Seibert M (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71–91

    Article  PubMed  CAS  Google Scholar 

  • Guan YF, Deng MC, Yu XJ, Zhang W (2004) Two-stage photo-biological production of hydrogen by marine green alga Platymonas subcordiformis. Biochem Eng J 19:69–73

    Article  CAS  Google Scholar 

  • Hackenberg C, Engelhardt A, Matthijs HCP, Wittink F, Bauwe H, Kaplan A, Hagemann M (2009) Photorespiratory 2-phosphoglycolate metabolism and photoreduction of O2 cooperate in high-light acclimation of Synechocystis sp strain PCC 6803. Planta 230:625–637

    Article  PubMed  CAS  Google Scholar 

  • Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269:1022–1032

    Article  PubMed  CAS  Google Scholar 

  • Healey FP (1970) Hydrogen evolution by several algae. Planta 91:220–226

    Article  CAS  Google Scholar 

  • Helman Y, Tchernov D, Reinhold L, Shibata M, Ogawa T, Schwarz R, Ohad I, Kaplan A (2003) Genes encoding a-type flavoproteins are essential for photoreduction of O2 in cyanobacteria. Curr Biol 13:230–235

    Article  PubMed  CAS  Google Scholar 

  • Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, Krieger-Liszkay A (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J Biol Chem 284:31174–31180

    Article  PubMed  CAS  Google Scholar 

  • Horvath EM, Peter SO, Joet T, Rumeau D, Cournac L, Horvath GV, Kavanagh TA, Schafer C, Peltier G, Medgyesy P (2000) Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol 123:1337–1349

    Article  PubMed  CAS  Google Scholar 

  • Howitt CA, Vermaas WFJ (1998) Quinol and cytochrome oxidases in the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry 37:17944–17951

    Article  PubMed  CAS  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamura A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213

    Article  PubMed  CAS  Google Scholar 

  • Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, Cuine S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P) H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci USA 105:20546–20551

    Article  PubMed  Google Scholar 

  • Joet T, Cournac L, Horvath EM, Medgyesy P, Peltier G (2001) Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol 125:1919–1929

    Article  PubMed  CAS  Google Scholar 

  • Joet T, Genty B, Josse EM, Kuntz M, Cournac L, Peltier G (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277:31623–31630

    Article  PubMed  CAS  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066

    Article  PubMed  CAS  Google Scholar 

  • Kitayama K, Kitayama M, Osafune T, Togasaki RK (1999) Subcellular localization of iron and manganese superoxide dismutase in Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 35:136–142

    Article  CAS  Google Scholar 

  • Krömer S (1995) Respiration during photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 46:45–70

    Article  Google Scholar 

  • Kruse O, Rupprecht J, Mussgnug JR, Dismukes GC, Hankamer B (2005) Photosynthesis: a blueprint for solar energy capture and biohydrogen production technologies. Photochem Photobiol Sci 4:957–970

    Article  PubMed  CAS  Google Scholar 

  • Lemaire C, Wollman FA, Bennoun P (1988) Restoration of phototrophic growth in a mutant of Chlamydomonas reinhardtii in which the chloroplast atpB gene of the ATP synthase has a deletion: an example of mitochondria-dependent photosynthesis. Proc Natl Acad Sci USA 85:1344–1348

    Article  PubMed  CAS  Google Scholar 

  • Lemieux C, Otis C, Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649–652

    Article  PubMed  CAS  Google Scholar 

  • Mackey KRM, Paytan A, Grossman AR, Bailey S (2008) A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnol Oceanog 53:900–913

    CAS  Google Scholar 

  • McDonald AE, Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Physiol 1:357–364

    Google Scholar 

  • McDonald AE, Amirsadeghi S, Vanlerberghe GC (2003) Prokaryotic orthologues of mitochondrial alternative oxidase and plastid terminal oxidase. Plant Mol Biol 53:865–876

    Article  PubMed  CAS  Google Scholar 

  • Mehler AH (1951) Studies on reactions of illuminated chloroplasts.1. Mechanism of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77

    Article  CAS  Google Scholar 

  • Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748

    Article  PubMed  CAS  Google Scholar 

  • Melis A, Zhang LP, 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 122:127–135

    Article  PubMed  CAS  Google Scholar 

  • Meuser JE, Ananyev G, Wittig LE, Kosourov S, Ghirardi ML, Seibert M, Dismukes GC, Posewitz MC (2009) Phenotypic diversity of hydrogen production in chlorophycean algae reflects distinct anaerobic metabolisms. J Biotechnol 142:21–30

    Article  PubMed  CAS  Google Scholar 

  • Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084

    Article  PubMed  CAS  Google Scholar 

  • Miyachi S, Iwasaki I, Shiraiwa Y (2003) Historical perspective on microalgal and cyanobacterial acclimation to low- and extremely high-CO2 conditions. Photosynth Res 77:139–153

    Article  PubMed  CAS  Google Scholar 

  • Moseley JL, Chang CW, Grossman AR (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell 5:26–44

    Article  PubMed  CAS  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    Article  PubMed  CAS  Google Scholar 

  • Munekage Y, Hashimoto M, Miyaka C, Tomizawa KI, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582

    Article  PubMed  CAS  Google Scholar 

  • Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708:322–332

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  PubMed  CAS  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  PubMed  CAS  Google Scholar 

  • Osmond CB (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98

    CAS  Google Scholar 

  • Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277:427–439

    Article  PubMed  CAS  Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Ann Rev Plant Physiol Plant Mol Biol 53:523–550

    CAS  Google Scholar 

  • Peltier G, Thibault P (1985) Oxygen uptake in the light in Chlamydomonas. Evidence for persistent mitochondrial respiration. Plant Physiol 79:225–230

    Article  PubMed  CAS  Google Scholar 

  • Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284:32770–32781

    Article  PubMed  CAS  Google Scholar 

  • Pombert JF, Lemieux C, Turmel M (2006) The complete chloroplast DNA sequence of the green alga Oltmannsiellopsis viridis reveals a distinctive quadripartite architecture in the chloroplast genome of early diverging ulvophytes. BMC Biol 4:3

    Article  PubMed  CAS  Google Scholar 

  • Radmer RJ, Kok B (1976) Photoreduction of O2 primes and replaces CO2 assimilation. Plant Physiol 58:336–340

    Article  PubMed  CAS  Google Scholar 

  • Ravenel J, Peltier G, Havaux M (1994) The cyclic electron pathways around photosystem-I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251–259

    Article  CAS  Google Scholar 

  • Roberts K, Granum E, Leegood RC, Raven JA (2007) Carbon acquisition by diatoms. Photosynth Res 93:79–88

    Article  PubMed  CAS  Google Scholar 

  • Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775

    Article  PubMed  CAS  Google Scholar 

  • Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, Maxwell DP, Huner NPA (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of arabidopsis during steady-state photosynthesis. Plant Physiol 142:574–585

    Article  PubMed  CAS  Google Scholar 

  • Rosso D, Bode R, Li WZ, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Huner NPA (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 21:3473–3492

    Article  PubMed  CAS  Google Scholar 

  • Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051

    Article  PubMed  CAS  Google Scholar 

  • Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368

    Article  PubMed  CAS  Google Scholar 

  • Shao N, Beck CF, Lemaire SD, Krieger-Liszkay A (2008) Photosynthetic electron flow affects H2O2 signaling by inactivation of catalase in Chlamydomonas reinhardtii. Planta 228:1055–1066

    Article  PubMed  CAS  Google Scholar 

  • Shelp BJ, Canvin DT (1980) Photo-respiration and oxygen inhibition of photosynthesis in Chlorella pyrenoidosa. Plant Physiol 65:780–784

    Article  PubMed  CAS  Google Scholar 

  • Skjanes K, Knutsen G, Kallqvist T, Lindblad P (2008) H2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design. Int J Hydrogen Energy 33:511–521

    Article  CAS  Google Scholar 

  • 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 106:17331–17336

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Sugiura C, Kobayashi Y, Aoki S, Sugita C, Sugita M (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nuc Acid Res 31:5324–5331

    Article  CAS  Google Scholar 

  • Suorsa M, Sirpio S, Aro EM (2009) Towards characterization of the chloroplast NAD(P)H dehydrogenase complex. Mol Plant 2:1127–1140

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Gagnon MC, O’Kelly CJ, Otis C, Lemieux C (2009) The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of Prasinophytes and the origin of the secondary chloroplasts of Euglenids. Mol Biol Evol 26:631–648

    Article  PubMed  CAS  Google Scholar 

  • Vicente JB, Gomes CM, Wasserfallen A, Teixeira M (2002) Module fusion in an A-type flavoprotein from the cyanobacterium Synechocystis condenses a multiple-component pathway in a single polypeptide chain. Biochem Biophys Res Commun 294:82–87

    Article  PubMed  CAS  Google Scholar 

  • Vicente JB, Scandurra FM, Forte E, Brunori M, Sarti P, Teixeira M, Giuffrè A, Robert KP (2008) Kinetic characterization of the Escherichia coli nitric oxide reductase flavorubredoxin. In Methods in enzymology, vol 437. Academic Press, pp 47–62

  • Vidi PA, Kanwischer M, Baginsky S, Austin JR, Csucs G, Dormann P, Kessler F, Brehelin C (2006) Tocopherol cyclase (VTE1) localization and vitamin E accumulation in chloroplast plastoglobule lipoprotein particles. J Biol Chem 281:11225–11234

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci USA 91:9794–9798

    Article  PubMed  CAS  Google Scholar 

  • Wakasugi T, Nagai T, Kapoor M, Sugita M, Ito M, Ito S, Tsudzuki J, Nakashima K, Tsudzuki T, Suzuki Y, Hamada A, Ohta T, Inamura A, Yoshinaga K, Sugiura M (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc Natl Acad Sci USA 94:5967–5972

    Article  PubMed  CAS  Google Scholar 

  • Wang JX, Sommerfeld M, Hu Q (2009) Occurrence and environmental stress responses of two plastid terminal oxidases in Haematococcus pluvialis (Chlorophyceae). Planta 230:191–203

    Article  PubMed  CAS  Google Scholar 

  • Winkler M, Hemschemeier A, Gotor C, Melis A, Happe T (2002) [Fe]-hydrogenases in green algae: photo-fermentation and hydrogen evolution under sulfur deprivation. Int J Hydrogen Energy 27:1431–1439

    Article  CAS  Google Scholar 

  • 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 284:36620–36627

    Article  PubMed  CAS  Google Scholar 

  • Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG (2005) The role and evolution of superoxide dismutases in algae. J Phycol 41:453–465

    Article  CAS  Google Scholar 

  • Wolfe-Simon F, Starovoytov V, Reinfelder JR, Schofield O, Falkowski PG (2006) Localization and role of manganese superoxide dismutase in a marine diatom. Plant Physiol 142:1701–1709

    Article  PubMed  CAS  Google Scholar 

  • Wu DY, Wright DA, Wetzel C, Voytas DF, Rodermel S (1999) The immutans variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11:43–55

    Article  PubMed  CAS  Google Scholar 

  • Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147:340–354

    Article  PubMed  CAS  Google Scholar 

  • Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WFJ, Havaux M, Matthijs HCP (2005) Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol 46:1433–1436

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Allahverdiyeva Y, Eisenhut M, Aro E-M (2009) Flavodiiron proteins in oxygenic photosynthetic organisms: photoprotection of photosystem II by Flv2 and Flv4 in Synechocystis sp. PCC 6803. PLoS ONE 4:e5331

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This study was supported by the European FP7-Energy-RTD program (SOLAR-H2 Project No. 212508), and by the French “Agence Nationale pour la Recherche” ALGOMICS project (ANR-08-BIO-002).

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Correspondence to Gilles Peltier.

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Peltier, G., Tolleter, D., Billon, E. et al. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106, 19–31 (2010). https://doi.org/10.1007/s11120-010-9575-3

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