Current Genetics

, Volume 57, Issue 3, pp 151–168 | Cite as

The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features

  • Mia Terashima
  • Michael Specht
  • Michael HipplerEmail author


The unicellular green alga Chlamydomonas reinhardtii has emerged to be an important model organism for the study of oxygenic eukaryotic photosynthesis as well as other processes occurring in the chloroplast. However, the chloroplast proteome in C. reinhardtii has only recently been comprehensively characterized, made possible by proteomics emerging as an accessible and powerful tool over the last decade. In this review, we introduce a compiled list of 996 experimentally chloroplast-localized proteins for C. reinhardtii, stemming largely from our previous proteomic dataset comparing chloroplasts and mitochondria samples to localize proteins. In order to get a taste of some cellular functions taking place in the C. reinhardtii chloroplast, we will focus this review particularly on metabolic differences between chloroplasts of C. reinhardtii and higher plants. Areas that will be covered are photosynthesis, chlorophyll biosynthesis, carbon metabolism, fermentative metabolism, ferredoxins and ferredoxin-interacting proteins.


Chlamydomonas reinhardtii Chloroplast proteome Photosynthesis Fermentation Metabolism Evolution 



We thank Christian Fufezan for his insightful input regarding the BLAST analyses. MT was supported by Deutscher Akademischer Austauschdienst (DAAD), Ph.D. fellowship. MH acknowledges support from the DFG, from the BMBF (BMBF 0315265 C, GOFORSYS partner) and FP7-funded Sunbiopath project (GA245070).

Supplementary material

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Supplementary material 1 (DOCX 17 kb)
294_2011_339_MOESM2_ESM.xls (330 kb)
Supplementary Table 1 (XLS 330 kb)


  1. Abdallah F, Salamini F, Leister D (2000) A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 5:141–142PubMedCrossRefGoogle Scholar
  2. Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85:15–32PubMedCrossRefGoogle Scholar
  3. Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proc Natl Acad Sci USA 107:11128–11133PubMedCrossRefGoogle Scholar
  4. Allmer J, Naumann B, Markert C, Zhang M, Hippler M (2006) Mass spectrometric genomic data mining: Novel insights into bioenergetic pathways in Chlamydomonas reinhardtii. Proteomics 6:6207–6220PubMedCrossRefGoogle Scholar
  5. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  6. Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature 447:58–63PubMedCrossRefGoogle Scholar
  7. Appel J, Schulz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis—hydrogenases as important regulatory devices for a proper redox poising? J Photochem Photobiol B Biol 47:1–11CrossRefGoogle Scholar
  8. Armstrong GA (1998) Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. J Photochem Photobiol B Biol 43:87–100CrossRefGoogle Scholar
  9. Atteia A, Adrait A, Brugiére S, Tardif M, van Lis R, Deusch O, Dagan T, Kuhn L, Gontero B, Martin W, Garin J, Joyard J, Rolland N (2009) A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor. Mol Biol Evol 26:1533–1548PubMedCrossRefGoogle Scholar
  10. Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, Martin W (2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281:9909–9918PubMedCrossRefGoogle Scholar
  11. Atteia A, van Lis R, Mendoza-Hernandez G, Henze K, Martin W, Riveros-Rosas H, Gonzalez-Halphen D (2003) Bifunctional aldehyde/alcohol dehydrogenase (ADHE) in chlorophyte algal mitochondria. Plant Mol Biol 53:175–188PubMedCrossRefGoogle Scholar
  12. Baginsky S (2009) Plant proteomics: concepts, applications, and novel strategies for data interpretation. Mass Spectrom Rev 28:93–120PubMedCrossRefGoogle Scholar
  13. Baginsky S, Gruissem W (2009) The chloroplast kinase network: new insights from large-scale phosphoproteome profiling. Mol Plant 2:1141–1153PubMedCrossRefGoogle Scholar
  14. Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895PubMedCrossRefGoogle Scholar
  15. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635PubMedCrossRefGoogle Scholar
  16. Blonde JD, Plaxton WC (2003) Structural and kinetic properties of high and low molecular mass phosphoenolpyruvate carboxylase isoforms from the endosperm of developing castor oilseeds. J Biol Chem 278:11867–11873PubMedCrossRefGoogle Scholar
  17. Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383PubMedCrossRefGoogle Scholar
  18. Busch A, Rimbauld B, Naumann B, Rensch S, Hippler M (2008) Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo-oxidative stress in response to iron availability in Chlamydomonas reinhardtii. Plant J 55:201–211PubMedCrossRefGoogle Scholar
  19. Cahoon AB, Timko MP (2000) yellow-in-the-dark mutants of Chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase. Plant Cell 12:559–568PubMedCrossRefGoogle Scholar
  20. Charon MH, Volbeda A, Chabriere E, Pieulle L, Fontecilla-Camps JC (1999) Structure and electron transfer mechanism of pyruvate:ferredoxin oxidoreductase. Curr Opin Struct Biol 9:663–669PubMedCrossRefGoogle Scholar
  21. Chen C, Gibbs M (1992a) Some enzymes and properties of the reductive carboxylic acid cycle are present in the green alga Chlamydomonas reinhardtii F-60. Plant Physiol 98:535–539PubMedCrossRefGoogle Scholar
  22. Chen C, Gibbs M (1992b) Coupling of carbon dioxide fixation to the oxyhydrogen reaction in the isolated chloroplast of Chlamydomonas reinhardtii. Plant Physiol 100:1361–1365PubMedCrossRefGoogle Scholar
  23. Chollet R, Vidal J, O’Leary MH (1996) PHOSPHOENOLPYRUVATE CARBOXYLASE: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47:273–298PubMedCrossRefGoogle Scholar
  24. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann D, 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 132:273–285PubMedCrossRefGoogle Scholar
  25. Dammeyer T, Hofmann E, Frankenberg-Dinkel N (2008) Phycoerythrobilin synthase (PebS) of a marine virus. Crystal structures of the biliverdin complex and the substrate-free form. J Biol Chem 283:27547–27554PubMedCrossRefGoogle Scholar
  26. Depége N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575PubMedCrossRefGoogle Scholar
  27. Desplats C, Mus F, Cuiné 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 284:4148–4157PubMedCrossRefGoogle Scholar
  28. Deusch O, Landan G, Roettger M, Gruenheit N, Kowallik KV, Allen JF, Martin W, Dagan T (2008) Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 25:748–761PubMedCrossRefGoogle Scholar
  29. 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 284:7201–7213PubMedCrossRefGoogle Scholar
  30. Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515PubMedCrossRefGoogle Scholar
  31. Elrad D, Grossman AR (2004) A genome’s-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr Genet 45:61–75PubMedCrossRefGoogle Scholar
  32. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971PubMedCrossRefGoogle Scholar
  33. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984PubMedCrossRefGoogle Scholar
  34. Embley TM (2006) Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos Trans R Soc Lond B Biol Sci 361:1055–1067PubMedCrossRefGoogle Scholar
  35. Embley TM, van der Giezen M, Horner DS, Dyal PL, Bell S, Foster PG (2003) Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55:387–395PubMedCrossRefGoogle Scholar
  36. Esper B, Badura A, Rogner M (2006) Photosynthesis as a power supply for (bio-)hydrogen production. Trends Plant Sci 11:543–549PubMedCrossRefGoogle Scholar
  37. Evans MC, Buchanan BB, Arnon DI (1966) A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA 55:928–934PubMedCrossRefGoogle Scholar
  38. Ferro M, Brugiére S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteom 9:1063–1084CrossRefGoogle Scholar
  39. 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 276:6125–6132PubMedCrossRefGoogle Scholar
  40. Flugge UI (1999) Phosphate translocators in plastids. Annu Rev Plant Physiol Plant Mol Biol 50:27–45PubMedCrossRefGoogle Scholar
  41. 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 270:2750–2758PubMedCrossRefGoogle Scholar
  42. Frankenberg N, Mukougawa K, Kohchi T, Lagarias JC (2001) Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13:965–978PubMedCrossRefGoogle Scholar
  43. Fujita Y, Takagi H, Hase T (1996) Identification of the chlB gene and the gene product essential for the light-independent chlorophyll biosynthesis in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 37:313–323PubMedGoogle Scholar
  44. Fukuda W, Ismail YS, Fukui T, Atomi H, Imanaka T (2005) Characterization of an archaeal malic enzyme from the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. Archaea 1:293–301PubMedCrossRefGoogle Scholar
  45. Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219–240PubMedCrossRefGoogle Scholar
  46. Gantt E, Edwards MR, Provasoli L (1971) Chloroplast structure of the Cryptophyceae. Evidence for phycobiliproteins within intrathylakoidal spaces. J Cell Biol 48:280–290PubMedCrossRefGoogle Scholar
  47. Germano M, Yakushevska AE, Keegstra W, van Gorkom HJ, Dekker JP, Boekema EJ (2002) Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii. FEBS Lett 525:121–125PubMedCrossRefGoogle Scholar
  48. Gfeller RP, Gibbs M (1984) Fermentative Metabolism of Chlamydomonas reinhardtii: I. Analysis of fermentative products from starch in dark and light. Plant Physiol 75:212–218PubMedCrossRefGoogle Scholar
  49. Ginger ML, McFadden GI, Michels PA (2010) Rewiring and regulation of cross-compartmentalized metabolism in protists. Philos Trans R Soc Lond B Biol Sci 365:831–845PubMedCrossRefGoogle Scholar
  50. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA (2003) An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 132:2126–2134PubMedCrossRefGoogle Scholar
  51. 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 71:2777–2781PubMedCrossRefGoogle Scholar
  52. Goksoyr J (1967) Evolution of eucaryotic cells. Nature 214:1161PubMedCrossRefGoogle Scholar
  53. Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz M, Seibert M (2010) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol. doi: 10.1111/j.1469-8137.2010.03534.x
  54. Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S, Spalding MH (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10:190–198PubMedCrossRefGoogle Scholar
  55. Grossman AR, Schaefer MR, Chiang GG, Collier JL (1993) The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749PubMedGoogle Scholar
  56. Han S, Tang R, Anderson LK, Woerner TE, Pei ZM (2003) A cell surface receptor mediates extracellular Ca(2+) sensing in guard cells. Nature 425:196–200PubMedCrossRefGoogle Scholar
  57. Happe T, Hemschemeier A, Winkler M, Kaminski A (2002) Hydrogenases in green algae: do they save the algae’s life and solve our energy problems? Trends Plant Sci 7:246–250PubMedCrossRefGoogle Scholar
  58. Happe T, Kaminski A (2002) Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269:1022–1032PubMedCrossRefGoogle Scholar
  59. Happe T, Naber JD (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481PubMedCrossRefGoogle Scholar
  60. Harris EH (2001) Chlamydomonas as a model organism. Annu Rev Plant Physiol Plant Mol Biol 52:363–406PubMedCrossRefGoogle Scholar
  61. Harris EH (2008) The life of an acetate flagellate, Chap 6. In: Harris EH, Stern DB, Witman G (eds) The Chlamydomonas sourcebook: introduction to Chlamydomonas and its laboratory use. Academic Press, New York, pp 159–210Google Scholar
  62. Hatch MD, Slack CR (1968) A new enzyme for the interconversion of pyruvate and phosphopyruvate and its role in the C4 dicarboxylic acid pathway of photosynthesis. Biochem J 106:141–146PubMedGoogle Scholar
  63. Hatchikian EC, Le Gall J (1970) Study of dicarboxylic acid and pyruvate metabolism in sulfate-reducing bacteria. II. Electron transport; final acceptors. Ann Inst Pasteur (Paris) 118:288–301Google Scholar
  64. Heazlewood JL, Verboom RE, Tonti-Filippini J, Small I, Millar AH (2007) SUBA: the Arabidopsis subcellular database. Nucl Acids Res 35:D213–D218PubMedCrossRefGoogle Scholar
  65. Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe T (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227:397–407PubMedCrossRefGoogle Scholar
  66. Hemschemeier A, Happe T (2005) The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. Biochem Soc Trans 33:39–41PubMedCrossRefGoogle Scholar
  67. Hess WR, Steglich C, Lichtle C, Partensky F (1999) Phycoerythrins of the oxyphotobacterium Prochlorococcus marinus are associated to the thylakoid membrane and are encoded by a single large gene cluster. Plant Mol Biol 40:507–521PubMedCrossRefGoogle Scholar
  68. 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 28:595–606PubMedCrossRefGoogle Scholar
  69. Hippler M, Redding K, Rochaix JD (1998) Chlamydomonas genetics, a tool for the study of bioenergetic pathways. Biochim Biophys Acta 1367:1–62PubMedCrossRefGoogle Scholar
  70. Horner DS, Hirt RP, Embley TM (1999) A single eubacterial origin of eukaryotic pyruvate: ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol Biol Evol 16:1280–1291PubMedGoogle Scholar
  71. Hug LA, Stechmann A, Roger AJ (2010) Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol 27:311–324PubMedCrossRefGoogle Scholar
  72. Im CS, Zhang Z, Shrager J, Chang CW, Grossman AR (2003) Analysis of light and CO(2) regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth Res 75:111–125PubMedCrossRefGoogle Scholar
  73. 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 464:1210–1213PubMedCrossRefGoogle Scholar
  74. Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329PubMedCrossRefGoogle Scholar
  75. 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 105:20546–20551PubMedCrossRefGoogle Scholar
  76. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Prog Lipid Res 49:128–158PubMedCrossRefGoogle Scholar
  77. 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 1777:410–416PubMedCrossRefGoogle Scholar
  78. Kargul J, Nield J, Barber J (2003) Three-dimensional reconstruction of a light-harvesting complex I-photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii. Insights into light harvesting for PSI. J Biol Chem 278:16135–16141PubMedCrossRefGoogle Scholar
  79. Kirilovsky D, Ohad I (1986) Functional assembly in vitro of phycobilisomes with isolated photosystem II particles of eukaryotic chloroplasts. J Biol Chem 261:12317–12323PubMedGoogle Scholar
  80. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjölander K, Gruissem W, Baginsky S (2004) The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol 14:354–362PubMedCrossRefGoogle Scholar
  81. Klein U (1987) Intracellular carbon partitioning in Chlamydomonas reinhardtii. Plant Physiol 85:892–897PubMedCrossRefGoogle Scholar
  82. Klein U, Betz A (1978) Fermentative metabolism of hydrogen-evolving Chlamydomonas moewusii. Plant Physiol 61:953–956PubMedCrossRefGoogle Scholar
  83. Klimmek F, Sjödin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140:793–804PubMedCrossRefGoogle Scholar
  84. Klock G, Kreuzberg K (1991) Compartmented metabolite pools in protoplasts from the green alga Chlamydomonas reinhardtii: changes after transition from aerobiosis to anaerobiosis in the dark. Biochim Biophys Acta 1073:410–415PubMedGoogle Scholar
  85. Koziol AG, Borza T, Ishida K, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816PubMedCrossRefGoogle Scholar
  86. Kreuzberg K (1984) Starch fermentation via a formate producing pathway in Chlamydomonas reinhardii, Chlorogonium elongatum and Chlorella fusca. Physiologia Plantarum 61:87–94CrossRefGoogle Scholar
  87. Kropat J, Tottey S, Birkenbihl RP, Depége N, Huijser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA 102:18730–18735PubMedCrossRefGoogle Scholar
  88. Lemeille S, Rochaix JD (2010) State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res 106:33–46PubMedCrossRefGoogle Scholar
  89. Li J, Goldschmidt-Clermont M, Timko MP (1993) Chloroplast-encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii. Plant Cell 5:1817–1829PubMedCrossRefGoogle Scholar
  90. Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395PubMedCrossRefGoogle Scholar
  91. Lindmark DG, Müller M (1973) Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 248:7724–7728PubMedGoogle Scholar
  92. MacColl R (1998) Cyanobacterial phycobilisomes. J Struct Biol 124:311–334PubMedCrossRefGoogle Scholar
  93. Mamedov TG, Moellering ER, Chollet R (2005) Identification and expression analysis of two inorganic C- and N-responsive genes encoding novel and distinct molecular forms of eukaryotic phosphoenolpyruvate carboxylase in the green microalga Chlamydomonas reinhardtii. Plant J 42:832–843PubMedCrossRefGoogle Scholar
  94. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251PubMedCrossRefGoogle Scholar
  95. Maul JE, Lilly JW, Cui L, dePamphilis CW, Miller W, Harris EH, Stern DB (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell 14:2659–2679PubMedCrossRefGoogle Scholar
  96. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086PubMedCrossRefGoogle Scholar
  97. Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748PubMedCrossRefGoogle Scholar
  98. Melis A, Seibert M, Ghirardi ML (2007) Hydrogen fuel production by transgenic microalgae. Adv Exp Med Biol 616:110–121PubMedCrossRefGoogle Scholar
  99. 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 122:127–136PubMedCrossRefGoogle Scholar
  100. Merchant SS, Allen MD, Kropat J, Moseley JL, Long JC, Tottey S, Terauchi AM (2006) Between a rock and a hard place: trace element nutrition in Chlamydomonas. Biochim Biophys Acta 1763:578–594PubMedCrossRefGoogle Scholar
  101. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250PubMedCrossRefGoogle Scholar
  102. Mitchell BF, Pedersen LB, Feely M, Rosenbaum JL, Mitchell DR (2005) ATP production in Chlamydomonas reinhardtii flagella by glycolytic enzymes. Mol Biol Cell 16:4509–4518PubMedCrossRefGoogle Scholar
  103. Moellering ER, Ouyang Y, Mamedov TG, Chollet R (2007) The two divergent PEP-carboxylase catalytic subunits in the green microalga Chlamydomonas reinhardtii respond reversibly to inorganic-N supply and co-exist in the high-molecular-mass, hetero-oligomeric Class-2 PEPC complex. FEBS Lett 581:4871–4876PubMedCrossRefGoogle Scholar
  104. Moseley J, Quinn J, Eriksson M, Merchant S (2000) The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii. EMBO J 19:2139–2151PubMedCrossRefGoogle Scholar
  105. Moseley JL, Chang CW, Grossman AR (2006) Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot Cell 5:26–44PubMedCrossRefGoogle Scholar
  106. Moseley JL, Page MD, Alder NP, Eriksson M, Quinn J, Soto F, Theg SM, Hippler M, Merchant S (2002) Reciprocal expression of two candidate di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell 14:673–688PubMedCrossRefGoogle Scholar
  107. Mozzo M, Mantelli M, Passarini F, Caffarri S, Croce R, Bassi R (2010) Functional analysis of Photosystem I light-harvesting complexes (Lhca) gene products of Chlamydomonas reinhardtii. Biochim Biophys Acta 1797:212–221PubMedCrossRefGoogle Scholar
  108. Müller M (1993) The hydrogenosome. J Gen Microbiol 139:2879–2889PubMedGoogle Scholar
  109. Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251PubMedCrossRefGoogle Scholar
  110. 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 1708:322–332PubMedCrossRefGoogle Scholar
  111. 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 282:25475–25486PubMedCrossRefGoogle Scholar
  112. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7:3964–3979PubMedCrossRefGoogle Scholar
  113. Nevalainen L, Hrdy I, Muller M (1996) Sequence of a Giardia lamblia gene coding for the glycolytic enzyme, pyruvate, phosphate dikinase. Mol Biochem Parasitol 77:217–223PubMedCrossRefGoogle Scholar
  114. Nield J, Redding K, Hippler M (2004) Remodeling of light-harvesting protein complexes in chlamydomonas in response to environmental changes. Eukaryot Cell 3:1370–1380PubMedCrossRefGoogle Scholar
  115. Nomura H, Komori T, Kobori M, Nakahira Y, Shiina T (2008) Evidence for chloroplast control of external Ca2+-induced cytosolic Ca2+ transients and stomatal closure. Plant J 53:988–998PubMedCrossRefGoogle Scholar
  116. Ohta S, Miyamoto K, Miura Y (1987) Hydrogen evolution as a consumption mode of reducing equivalents in green algal fermentation. Plant Physiol 83:1022–1026PubMedCrossRefGoogle Scholar
  117. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521PubMedCrossRefGoogle Scholar
  118. Peltier G, Tolleter D, Billon E, Cournac L (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth Res 106:19–31PubMedCrossRefGoogle Scholar
  119. Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ (2004) New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. J Biol Chem 279:49367–49383PubMedCrossRefGoogle Scholar
  120. Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T (2009) Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21:3623–3640PubMedCrossRefGoogle Scholar
  121. 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 284:32770–32781PubMedCrossRefGoogle Scholar
  122. Pinta V, Picaud M, Reiss-Husson F, Astier C (2002) Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184:746–753PubMedCrossRefGoogle Scholar
  123. Posewitz MC, King PW, Smolinski SL, Zhang L, Seibert M, Ghirardi ML (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720PubMedCrossRefGoogle Scholar
  124. 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 275:6080–6089Google Scholar
  125. Ragsdale SW (2003) Pyruvate ferredoxin oxidoreductase and its radical intermediate. Chem Rev 103:2333–2346PubMedCrossRefGoogle Scholar
  126. Reeves RE (1968) A new enzyme with the glycolytic function of pyruvate kinase. J Biol Chem 243:3202–3204PubMedGoogle Scholar
  127. Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150:889–903PubMedCrossRefGoogle Scholar
  128. Rivoal J, Plaxton WC, Turpin DH (1998) Purification and characterization of high- and low-molecular-mass isoforms of phosphoenolpyruvate carboxylase from Chlamydomonas reinhardtii. Kinetic, structural and immunological evidence that the green algal enzyme is distinct from the prokaryotic and higher plant enzymes. Biochem J 331:201–209PubMedGoogle Scholar
  129. Rivoal J, Trzos S, Gage DA, Plaxton WC, Turpin DH (2001) Two unrelated phosphoenolpyruvate carboxylase polypeptides physically interact in the high molecular mass isoforms of this enzyme in the unicellular green alga Selenastrum minutum. J Biol Chem 276:12588–12597PubMedCrossRefGoogle Scholar
  130. Rochaix J, Fischer N, Hippler M (2000) Chloroplast site-directed mutagenesis of photosystem I in Chlamydomonas: electron transfer reactions and light sensitivity. Biochimie 82:635–645PubMedCrossRefGoogle Scholar
  131. Rolland N, Atteia A, Decottignies P, Garin J, Hippler M, Kreimer G, Lemaire SD, Mittag M, Wagner V (2009) Chlamydomonas proteomics. Curr Opin Microbiol 12:285–291PubMedCrossRefGoogle Scholar
  132. Rosenthal B, Mai Z, Caplivski D, Ghosh S, de la Vega H, Graf T, Samuelson J (1997) Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J Bacteriol 179:3736–3745PubMedGoogle Scholar
  133. Rotte C, Stejskal F, Zhu G, Keithly JS, Martin W (2001) Pyruvate:NADP+ oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol Biol Evol 18:710–720PubMedGoogle Scholar
  134. Rumpho ME, Edwards GE (1984) Inhibition of 3-Phosphoglycerate-Dependent O(2) Evolution by Phosphoenolpyruvate in C(4) Mesophyll Chloroplasts of Digitaria sanguinalis (L.) Scop. Plant Physiol 76:711–718PubMedCrossRefGoogle Scholar
  135. Schmidt M, Gessner G, Luff M, Heiland I, Wagner V, Kaminski M, Geimer S, Eitzinger N, Reissenweber T, Voytsekh O, Fiedler M, Mittag M, Kreimer G (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements. Plant Cell 18:1908–1930PubMedCrossRefGoogle Scholar
  136. Schutz K, Happe T, Troshina O, Lindblad P, Leitao E, Oliveira P, Tamagnini P (2004) Cyanobacterial H(2) production—a comparative analysis. Planta 218:350–359PubMedCrossRefGoogle Scholar
  137. Slamovits CH, Keeling PJ (2006) Pyruvate-phosphate dikinase of oxymonads and parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryot Cell 5:148–154PubMedCrossRefGoogle Scholar
  138. Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, Giedroc DP, Merchant SS (2010) The CRR1 nutritional copper sensor in chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22:4098–4113PubMedCrossRefGoogle Scholar
  139. Stauber EJ, Busch A, Naumann B, Svatos A, Hippler M (2009) Proteotypic profiling of LHCI from Chlamydomonas reinhardtii provides new insights into structure and function of the complex. Proteomics 9:398–408PubMedCrossRefGoogle Scholar
  140. Stauber EJ, Fink A, Markert C, Kruse O, Johanningmeier U, Hippler M (2003) Proteomics of Chlamydomonas reinhardtii light-harvesting proteins. Eukaryot Cell 2:978–994PubMedCrossRefGoogle Scholar
  141. Steglich C, Behrenfeld M, Koblizek M, Claustre H, Penno S, Prasil O, Partensky F, Hess WR (2001) Nitrogen deprivation strongly affects photosystem II but not phycoerythrin level in the divinyl-chlorophyll b-containing cyanobacterium Prochlorococcus marinus. Biochim Biophys Acta 1503:341–349PubMedCrossRefGoogle Scholar
  142. Steglich C, Frankenberg-Dinkel N, Penno S, Hess WR (2005) A green light-absorbing phycoerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp. MED4. Environ Microbiol 7:1611–1618PubMedCrossRefGoogle Scholar
  143. Steglich C, Mullineaux CW, Teuchner K, Hess WR, Lokstein H (2003) Photophysical properties of Prochlorococcus marinus SS120 divinyl chlorophylls and phycoerythrin in vitro and in vivo. FEBS Lett 553:79–84PubMedCrossRefGoogle Scholar
  144. Sun Q, Zybailov B, Majeran W, Friso G, Olinares PD, van Wijk KJ (2009) PPDB, the plant proteomics database at cornell. Nucl Acids Res 37:D969–D974PubMedCrossRefGoogle Scholar
  145. Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482PubMedCrossRefGoogle Scholar
  146. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteom 9:1514–1532CrossRefGoogle Scholar
  147. 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 284:25867–25878PubMedCrossRefGoogle Scholar
  148. Terauchi AM, Peers G, Kobayashi MC, Niyogi KK, Merchant SS (2010) Trophic status of Chlamydomonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth Res 105:39–49PubMedCrossRefGoogle Scholar
  149. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939PubMedCrossRefGoogle Scholar
  150. Timko MP (1998) Pigment biosynthesis: chlorophylls, heme, and carotenoids. In: Rochaix MG-C JD, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer, The Netherlands, pp 377–414Google Scholar
  151. Tokutsu R, Iwai M, Minagawa J (2009) CP29, a monomeric light-harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J Biol Chem 284:7777–7782PubMedCrossRefGoogle Scholar
  152. Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S, Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100:16119–16124PubMedCrossRefGoogle Scholar
  153. Vainonen JP, Sakuragi Y, Stael S, Tikkanen M, Allahverdiyeva Y, Paakkarinen V, Aro E, Suorsa M, Scheller HV, Vener AV, Aro EM (2008) Light regulation of CaS, a novel phosphoprotein in the thylakoid membrane of Arabidopsis thaliana. FEBS J 275:1767–1777PubMedCrossRefGoogle Scholar
  154. Vanlerberghe GC, Feil R, Turpin DH (1990) Anaerobic metabolism in the N-Limited Green Alga Selenastrum minutum: I. Regulation of carbon metabolism and succinate as a fermentation product. Plant Physiol 94:1116–1123PubMedCrossRefGoogle Scholar
  155. Vanlerberghe GC, Horsey AK, Weger HG, Turpin DH (1989) Anaerobic carbon metabolism by the tricarboxylic acid cycle: evidence for partial oxidative and reductive pathways during dark ammonium assimilation. Plant Physiol 91:1551–1557PubMedCrossRefGoogle Scholar
  156. Wagner V, Kreimer G, Mittag M (2008) The power of functional proteomics: components of the green algal eyespot and its light signaling pathway(s). Plant Signal Behav 3:433–435PubMedCrossRefGoogle Scholar
  157. Wahl RC, Orme-Johnson WH (1987) Clostridial pyruvate oxidoreductase and the pyruvate-oxidizing enzyme specific to nitrogen fixation in Klebsiella pneumoniae are similar enzymes. J Biol Chem 262:10489–10496PubMedGoogle Scholar
  158. Weaver PF, Lien S, Seibert M (1980) Photobiological production of hydrogen. Solar Energy 24:3–45CrossRefGoogle Scholar
  159. Weinl S, Held K, Schlucking K, Steinhorst L, Kuhlgert S, Hippler M, Kudla J (2008) A plastid protein crucial for Ca2+-regulated stomatal responses. New Phytol 179:675–686PubMedCrossRefGoogle Scholar
  160. Whitney LA, Loreti E, Alpi A, Perata P (2010) Alcohol dehydrogenase and hydrogenase transcript fluctuations during a day-night cycle in Chlamydomonas reinhardtii: the role of anoxia. New Phytol 190:488–498PubMedCrossRefGoogle Scholar
  161. Wienkoop S, Baginsky S, Weckwerth W (2010) Arabidopsis thaliana as a model organism for plant proteome research. J Proteomics 73:2239–2248PubMedCrossRefGoogle Scholar
  162. Winkler M, Hemschemeier A, Jacobs J, Stripp S, Happe T (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii—their role under stress conditions and biotechnological implications. Eur J Cell Biol 89:998–1004PubMedCrossRefGoogle Scholar
  163. Wu SH, McDowell MT, Lagarias JC (1997) Phycocyanobilin is the natural precursor of the phytochrome chromophore in the green alga Mesotaenium caldariorum. J Biol Chem 272:25700–25705PubMedCrossRefGoogle Scholar
  164. Xu P, Widmer G, Wang Y, Ozaki LS, Alves JM, Serrano MG, Puiu D, Manque P, Akiyoshi D, Mackey AJ, Pearson WR, Dear PH, Bankier AT, Peterson DL, Abrahamsen MS, Kapur V, Tzipori S, Buck GA (2004) The genome of Cryptosporidium hominis. Nature 431:1107–1112PubMedCrossRefGoogle Scholar
  165. Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, JRr Yates, Mayfield SP (2003) Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome. Identification of proteins unique to th e70 S ribosome. J Biol Chem 278:33774–33785PubMedCrossRefGoogle Scholar
  166. Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, JRr Yates, Mayfield SP (2002) Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell 14:2957–2974PubMedCrossRefGoogle Scholar
  167. Yamaguchi K, Subramanian AR (2000) The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275:28466–28482PubMedCrossRefGoogle Scholar
  168. Yamaguchi K, von Knoblauch K, Subramanian AR (2000) The plastid ribosomal proteins. Identification of all the proteins in the 30 S subunit of an organelle ribosome (chloroplast). J Biol Chem 275:28455–28465PubMedCrossRefGoogle Scholar
  169. Yamamoto H, Kurumiya S, Ohashi R, Fujita Y (2009) Oxygen sensitivity of a nitrogenase-like protochlorophyllide reductase from the cyanobacterium Leptolyngbya boryana. Plant Cell Physiol 50:1663–1673PubMedCrossRefGoogle Scholar
  170. Yamazaki S, Nomata J, Fujita Y (2006) Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. Plant Physiol 142:911–922PubMedCrossRefGoogle Scholar
  171. Yoon KS, Hille R, Hemann C, Tabita FR (1999) Rubredoxin from the green sulfur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J Biol Chem 274:29772–29778PubMedCrossRefGoogle Scholar
  172. Yu QB, Li G, Wang G, Sun JC, Wang PC, Wang C, Mi HL, Ma WM, Cui J, Cui YL, Chong K, Li YX, Li YH, Zhao Z, Shi TL, Yang ZN (2008) Construction of a chloroplast protein interaction network and functional mining of photosynthetic proteins in Arabidopsis thaliana. Cell Res 18:1007–1019PubMedCrossRefGoogle Scholar
  173. Zappa S, Li K, Bauer CE (2010) The tetrapyrrole biosynthetic pathway and its regulation in Rhodobacter capsulatus. Adv Exp Med Biol 675:229–250PubMedCrossRefGoogle Scholar
  174. Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348PubMedCrossRefGoogle Scholar
  175. Zhaxybayeva O, Doolittle WF, Papke RT, Gogarten JP (2009) Intertwined evolutionary histories of marine Synechococcus and Prochlorococcus marinus. Genome Biol Evol 1:325–339PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Mia Terashima
    • 1
  • Michael Specht
    • 1
  • Michael Hippler
    • 1
    Email author
  1. 1.Department of Biology, Institute of Plant Biology and BiotechnologyUniversity of MünsterMünsterGermany

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