Chlamydomonas reinhardtii chloroplasts contain a homodimeric pyruvate: Ferredoxin oxidoreductase that functions with FDX1

Plant Physiology

Volumn 161, Issue 1, 2013, Pages 57-71

  van Lis, Robert ^a   Baffert, Carole ^a   Couté, Yohann ^b,c,d   Nitschke, Wolfgang ^a   Atteia, Ariane ^a  

^a CNRS   (France)

^b CEA GRENOBLE   (France)

^c INSERM   (France)

^d UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; CHLAMYDOMONAS REINHARDTII; ESCHERICHIA COLI; EUKARYOTA; PROTISTA;

EID: 84871779491     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.208181     Document Type: Article

References (79)

1. Akhmanova A, Voncken FG, Hosea KM, Harhangi H, Keltjens JT, op den Camp HJ, Vogels GD, Hackstein JH (1999) A hydrogenosome with pyruvate formate-lyase: anaerobic chytrid fungi use an alternative route for pyruvate catabolism. Mol Microbiol 32: 1103-1114
2. Atteia A, van Lis R, Gelius-Dietrich G, Adrait A, Garin J, Joyard J, Rolland N, MartinW(2006) Pyruvate formate-lyase and a novel route of eukaryotic ATP synthesis in Chlamydomonas mitochondria. J Biol Chem 281: 9909-9918
3. Atteia A, van Lis R, Tielens AGM, Martin WF (2012) Anaerobic energy metabolism in unicellular photosynthetic eukaryotes. Biochim Biophys Acta (in press)
4. Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LA, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17: 129-138
5. Blamey JM, Adams MW (1993) Purification and characterization of pyruvate ferredoxin oxidoreductase from the hyperthermophilic archaeon Pyrococcus furiosus. Biochim Biophys Acta 1161: 19-27
6. Blamey JM, Adams MW (1994) Characterization of an ancestral type of pyruvate ferredoxin oxidoreductase from the hyperthermophilic bacterium, Thermotoga maritima. Biochemistry 33: 1000-1007
7. Blaschkowski HP, Neuer G, Ludwig-Festl M, Knappe J (1982) Routes of flavodoxin and ferredoxin reduction in Escherichia coli: CoA-acylating pyruvate: flavodoxin and NADPH:flavodoxin oxidoreductases participating in the activation of pyruvate formate-lyase. Eur J Biochem 123: 563-569
8. Bock AK, Kunow J, Glasemacher J, Schönheit P (1996) Catalytic properties, molecular composition and sequence alignments of pyruvate:ferredoxin oxidoreductase from the methanogenic archaeon Methanosarcina barkeri (strain Fusaro). Eur J Biochem 237: 35-44
9. Castruita M, Casero D, Karpowicz SJ, Kropat J, Vieler A, Hsieh SI, Yan W, Cokus S, Loo JA, Benning C, et al (2011) Systems biology approach in Chlamydomonas reveals connections between copper nutrition and multiple metabolic steps. Plant Cell 23: 1273-1292
10. Catalanotti C, Dubini A, Subramanian V, Yang W, Magneschi L, Mus F, Seibert M, Posewitz MC, Grossman AR (2012) Altered fermentative metabolism in Chlamydomonas reinhardtii mutants lacking pyruvate formate lyase and both pyruvate formate lyase and alcohol dehydrogenase. Plant Cell 24: 692-707
11. Cavazza C, Contreras-Martel C, Pieulle L, Chabrière E, Hatchikian EC, Fontecilla-Camps JC (2006) Flexibility of thiamine diphosphate revealed by kinetic crystallographic studies of the reaction of pyruvateferredoxin oxidoreductase with pyruvate. Structure 14: 217-224
12. Chabrière E, Charon MH, Volbeda A, Pieulle L, Hatchikian EC, Fontecilla-Camps JC (1999) Crystal structures of the key anaerobic enzyme pyruvate:ferredoxin oxidoreductase, free and in complex with pyruvate. Nat Struct Biol 6: 182-190
13. 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: 663-669
14. de Sousa CAF, Sodek L (2003) Alanine metabolism and alanine aminotransferase activity in soybean (Glycine max) during hypoxia of the root system and subsequent return to normoxia. Environ Exp Bot 50: 1-8
15. Dupierris V, Masselon C, Court M, Kieffer-Jaquinod S, Bruley C (2009) A toolbox for validation of mass spectrometry peptides identification and generation of database: IRMa. Bioinformatics 25: 1980-1981
16. Durrant I (1990) Light-based detection of biomolecules. Nature 346:297-298
17. Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42: 463-515
18. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440: 623-630
19. Fuchs G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu Rev Microbiol 65: 631-658
20. Gelius-Dietrich G, Henze K (2004) Pyruvate formate lyase (PFL) and PFL activating enzyme in the chytrid fungus Neocallimastix frontalis: a freeradical enzyme system conserved across divergent eukaryotic lineages. J Eukaryot Microbiol 51: 456-463
21. 2-production. Appl Biochem Biotechnol 63-65: 141-151
22. Grossman AR, Catalanotti C, Yang W, Dubini A, Magneschi L, Subramanian V, Posewitz MC, Seibert M (2011) Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii. New Phytol 190: 279-288
23. 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: 190-198
24. Grossman AR, Harris EE, Hauser C, Lefebvre PA, Martinez D, Rokhsar D, Shrager J, Silflow CD, Stern D, Vallon O, et al (2003) Chlamydomonas reinhardtii at the crossroads of genomics. Eukaryot Cell 2: 1137-1150
25. Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222: 769-774
26. Harris E (1989) The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego
27. Hawkins CF, Borges A, Perham RN (1989) A common structural motif in thiamin pyrophosphate-binding enzymes. FEBS Lett 255: 77-82
28. Heifetz PB, Förster B, Osmond CB, Giles LJ, Boynton JE (2000) Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol 122: 1439-1445
29. Hemschemeier A, Jacobs J, Happe T (2008) Biochemical and physiological characterization of the pyruvate formate-lyase Pfl1 of Chlamydomonas reinhardtii, a typically bacterial enzyme in a eukaryotic alga. Eukaryot Cell 7: 518-526
30. 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: 1280-1291
31. Hrdý I, Müller M (1995) Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J Mol Evol 41: 388-396
32. Hug LA, Stechmann A, Roger AJ (2010) Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol 27: 311-324
33. +-dependent pyruvate dehydrogenase in mitochondria of Euglena gracilis. J Biochem 96: 931-934
34. Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583: 325-329
35. Kerscher L, Oesterhelt D (1981) Purification and properties of two 2-oxoacid: ferredoxin oxidoreductases from Halobacterium halobium. Eur J Biochem 116: 587-594
36. Kletzin A, Adams MW (1996) Molecular and phylogenetic characterization of pyruvate and 2-ketoisovalerate ferredoxin oxidoreductases from Pyrococcus furiosus and pyruvate ferredoxin oxidoreductase from Thermotoga maritima. J Bacteriol 178: 248-257
37. Knappe J, Sawers G (1990) A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. FEMS Microbiol Rev 6: 383-398
38. Knappe J, Schacht J, Möckel W, Höpner T, Vetter H Jr, Edenharder R (1969) Pyruvate formate-lyase reaction in Escherichia coli: the enzymatic system converting an inactive form of the lyase into the catalytically active enzyme. Eur J Biochem 11: 316-327
39. Kreuzberg K (1984) Starch fermentation via a formate producing pathway in Chlamydomonas reinhardtii, Chlorogonium elongatum and Chlorella fusca. Physiol Plant 61: 87-94
40. Kunow J, Linder D, Thauer RK (1995) Pyruvate:ferredoxin oxidoreductase from the sulfate-reducing Archaeoglobus fulgidus: molecular composition, catalytic properties, and sequence alignments. Arch Microbiol 163: 21-28
41. Lantsman Y, Tan KSW, Morada M, Yarlett N (2008) Biochemical characterization of a mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154: 2757-2766
42. 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: 7724-7728
43. Magneschi L, Catalanotti C, Subramanian V, Dubini A, Yang W, Mus F, Posewitz MC, Seibert M, Perata P, Grossman AR (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol 158: 1293-1305
44. Martin W (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 365: 847-855
45. Meinecke B, Bertram J, Gottschalk G (1989) Purification and characterization of the pyruvate-ferredoxin oxidoreductase from Clostridium acetobutylicum. Arch Microbiol 152: 244-250
46. Menon S, Ragsdale SW (1997) Mechanism of the Clostridium thermoaceticum pyruvate:ferredoxin oxidoreductase: evidence for the common catalytic intermediacy of the hydroxyethylthiamine pyropyrosphate radical. Biochemistry 36: 8484-8494
47. 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: 578-594
48. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu RY, van der Giezen M, Tielens AG, Martin WF (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76: 444-495
49. 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: 25475-25486
50. Nakamura M, Saeki K, Takahashi Y (1999) Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hs cA-fdx-ORF3 gene cluster. J Biochem 126: 10-18
51. Nguyen HM, Baudet M, Cuiné S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, et al (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11: 4266-4273
52. Page MD, Allen MD, Kropat J, Urzica EI, Karpowicz SJ, Hsieh SI, Loo JA, Merchant SS (2012) Fe sparing and Fe recycling contribute to increased superoxide dismutase capacity in iron-starved Chlamydomonas reinhardtii. Plant Cell 24: 2649-2665
53. Philipps G, Krawietz D, Hemschemeier A, Happe T (2011) A pyruvate formate lyase-deficient Chlamydomonas reinhardtii strain provides evidence for a link between fermentation and hydrogen production in green algae. Plant J 66: 330-340
54. Pieulle L, Guigliarelli B, Asso M, Dole F, Bernadac A, Hatchikian EC (1995) Isolation and characterization of the pyruvate-ferredoxin oxidoreductase from the sulfate-reducing bacterium Desulfovibrio africanus. Biochim Biophys Acta 1250: 49-59
55. Pieulle L, Magro V, Hatchikian EC (1997) Isolation and analysis of the gene encoding the pyruvate-ferredoxin oxidoreductase of Desulfovibrio africanus, production of the recombinant enzyme in Escherichia coli, and effect of carboxy-terminal deletions on its stability. J Bacteriol 179: 5684-5692
56. Pieulle L, Nouailler M, Morelli X, Cavazza C, Gallice P, Blanchet S, Bianco P, Guerlesquin F, Hatchikian EC (2004) Multiple orientations in a physiological complex: the pyruvate-ferredoxin oxidoreductaseferredoxin system. Biochemistry 43: 15480-15493
57. Plaga W, Lottspeich F, Oesterhelt D (1992) Improved purification, crystallization and primary structure of pyruvate:ferredoxin oxidoreductase from Halobacterium halobium. Eur J Biochem 205: 391-397
58. Rochaix JD (2002) The three genomes of Chlamydomonas. Photosynth Res 73: 285-293
59. + 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: 710-720
60. Rydzak T, Levin DB, Cicek N, Sparling R (2011) End-product induced metabolic shifts in Clostridium thermocellum ATCC 27405. Appl Microbiol Biotechnol 92: 199-209
61. Schägger H (2001) Blue-native gels to isolate protein complexes from mitochondria. Methods Cell Biol 65: 231-244
62. Schmitter JM, Jacquot JP, de Lamotte-Guéry F, Beauvallet C, Dutka S, Gadal P, Decottignies P (1988) Purification, properties and complete amino acid sequence of the ferredoxin from a green alga, Chlamydomonas reinhardtii. Eur J Biochem 172: 405-412
63. Spreitzer RJ, Mets LJ (1980) Non-mendelian mutation affecting ribulose-1,5-biphosphate carboxylase structure and activity. Nature 285: 114-115
64. Stairs CW, Roger AJ, Hampl V (2011) Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a Firmicute. Mol Biol Evol 28: 2087-2099
65. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234
66. Tardif M, Atteia A, Specht M, Cogne G, Rolland N, Brugière S, Hippler M, Ferro M, Bruley C, Peltier G, et al (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29: 3625-3639
67. Terashima M, Specht M, Naumann B, Hippler M (2010) Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol Cell Proteomics 9: 1514-1532
68. Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, et al (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284: 25867-25878
69. Townson SM, Upcroft JA, Upcroft P (1996) Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol Biochem Parasitol 79: 183-193
70. Uyeda K, Rabinowitz JC (1971) Pyruvate-ferredoxin oxidoreductase. 3. Purification and properties of the enzyme. J Biol Chem 246: 3111-3119
71. van Lis R, Atteia A, Nogaj LA, Beale SI (2005) Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii. Plant Physiol 139: 1946-1958
72. Verhaart MR, Bielen AA, van der Oost J, Stams AJ, Kengen SW (2010) Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal. Environ Technol 31: 993-1003
73. Vita N, Hatchikian EC, Nouailler M, Dolla A, Pieulle L (2008) Disulfide bond-dependent mechanism of protection against oxidative stress in pyruvate-ferredoxin oxidoreductase of anaerobic Desulfovibrio bacteria. Biochemistry 47: 957-964
74. Wagner AF, Frey M, Neugebauer FA, Schäfer W, Knappe J (1992) The free radical in pyruvate formate-lyase is located on glycine-734. Proc Natl Acad Sci USA 89: 996-1000
75. 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: 10489-10496
76. Wessel D, Flügge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138: 141-143
77. Williams K, Lowe PN, Leadlay PF (1987) Purification and characterization of pyruvate:ferredoxin oxidoreductase from the anaerobic protozoon Trichomonas vaginalis. Biochem J 246: 529-536
78. 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: 998-1004
79. 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