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Structure and Physiological Function of NDH-1 Complexes in Cyanobacteria

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Bioenergetic Processes of Cyanobacteria

Abstract

The metabolic flexibility of cyanobacteria has enabled them to survive and flourish under a wide range of environmental conditions. In particular their ability to perform oxygenic photosynthesis and respiration within the same cell has allowed them to generate ATP from diverse energy sources. While great strides have been made in understanding the molecular details of the photosynthetic apparatus in cyanobacteria, much less is known about the protein complexes involved in respiration. Here we review our current knowledge of cyanobacterial NDH-1 complexes. which are related to the type-I NADH dehydrogenase (NADH:quinone oxidoreductase) found in mitochondria and in other types of bacteria. The picture that is emerging from a combination of molecular biology, biochemistry, proteomics and structural biology is that cyanobacteria synthesize different types of NDH-1 complex depending on the physiological needs of the cell, and that cyanobacterial NDH-1 complexes play important physiological roles not only in respiration but also in cyclic electron flow around Photosystem I in the light and in the uptake of CO2 into the cell. These differences in function are reflected by differences in the subunit composition of the different types of NDH-1 complex. The subunit compositions of the cyanobacterial NDH-1 complexes and the closely related Ndh (or NDH) complex in chloroplasts suggest that they form a separate sub-class of the complex I family of enzymes. However, there are important differences between the NDH-1 class of complexes in chloroplasts and cyanobacteria, which appear to reflect adaptations that have occurred since their evolutionary divergence.

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References

  • Alpes I, Scherer S and Böger P (1989) The respiratory NADH dehydrogenase of the cyanobacterium Anabaena variabilis: purification and characterization. Biochim Biophys Acta 973: 41–46

    Article  CAS  Google Scholar 

  • Appel J and Schulz R (1996) Sequence analysis of an operon of a NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NAD(P)H-dehydrogenase (complex I). Biochim Biophys Acta 1298: 141–147

    Article  PubMed  CAS  Google Scholar 

  • Arteni AA, Zhang P, Battchikova N, Ogawa T, Aro E-M, Boekema EJ (2006) Structural characterization of the NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochim Biophys Acta 1757: 1469–1475

    Article  PubMed  CAS  Google Scholar 

  • Badger MR and Price GD (2003) CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54: 609–622

    Article  PubMed  CAS  Google Scholar 

  • Badger MR and Spalding MH (2000) CO2 acquisition, concentration and fixation in cyanobacteria and algae. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 369–397. Kluwer Academy Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Badger MR, Hanson D and Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29: 161–173

    Article  CAS  Google Scholar 

  • Badger MR, Price GD, Long BM and Woodger FJ (2006) The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. J Exp Bot 57: 249–265

    Article  PubMed  CAS  Google Scholar 

  • Battchikova N and Aro E-M (2007) Cyanobacterial NDH-1 complexes: multiplicity in function and subunit composition. Physiol Plant 131: 22–32

    Article  PubMed  CAS  Google Scholar 

  • Battchikova N, Zhang P, Rudd S, Ogawa T and Aro E-M (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1 M complexes of Synechocystis sp. PCC 6803. J Biol Chem 280: 2587–2595

    Article  PubMed  CAS  Google Scholar 

  • Bäumer S, Ide T, Jacobi C, Johann A, Gottschalk G and Deppenmeier U (2000) The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases. J Biol Chem 275: 17968–17973

    Article  PubMed  Google Scholar 

  • Berger S, Ellersiek U and Steinmüller K (1991) Cyanobacteria contain a mitochondrial complex I-homologous NADH-dehydrogenase. FEBS Lett 286: 129–132

    Article  PubMed  CAS  Google Scholar 

  • Berger S, Ellersiek U, Kinzelt D and Steinmüller K (1993) Immunopurification of a subcomplex of the NAD(P)H-plastoquinone-oxidoreductase from the cyanobacterium Synechocystis sp. PCC6803. FEBS Lett 326: 246–250

    Article  PubMed  CAS  Google Scholar 

  • Brandt U (2006) Energy converting NADH:quinone oxidoreductase (Complex I). Annu Rev Biochem 75: 69–92

    Article  PubMed  CAS  Google Scholar 

  • Burrows PA, Sazanov LA, Svab Z, Maliga P and Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868–876

    Article  PubMed  CAS  Google Scholar 

  • Carroll J, Fearnley IM, Skehel JM, Shannon RJ, Hirst J and Walker JE (2006) Bovine complex I is a complex of 45 different subunits. J Biol Chem 281: 32724–32727

    Article  PubMed  CAS  Google Scholar 

  • Cooley JW and Vermaas WFJ (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J Bacteriol 183: 4251–4258

    Article  PubMed  CAS  Google Scholar 

  • Deng Y, Ye J, Mi H and Shen Y (2003a) Separation of hydrophobic NAD(P)H dehydrogenase subcomplexes from cyanobacterium Synechocystis PCC6803. Acta Biochim Biophys Sinica 35: 723–727

    CAS  Google Scholar 

  • Deng Y, Ye J and Mi H (2003b) Effects of low CO2 on NAD(P)H dehydrogenase, a mediator of cyclic electron transport around photosystem I in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 44: 534–540

    Article  CAS  Google Scholar 

  • Dworsky A, Mayer B, Regelsberger G, Fromwald S and Peschek GA (1995) Functional and immunological characterization of both “mitochondria-like” and “chloroplast-like” electron/proton transport proteins in isolated and purified cyanobacterial membranes. Bioelectrochem Bioenerg 38: 35–43

    Article  CAS  Google Scholar 

  • Efremov RG, Baradaran R and Sazanov LA (2010) The architecture of complex I. Nature 465: 441–447

    Article  PubMed  CAS  Google Scholar 

  • Eisenhut M, von Wobeser EA, Jonas L, Schubert H, Ibelings BW, Bauwe H, Matthijs HCP and Hagemann M (2007) Long-term response toward inorganic carbon limitation in wild type and glycolate turnover mutants of the cyanobacterium Synechocystis sp. Strain PCC 6803. Plant Physiol 144: 1946–1959

    Article  PubMed  CAS  Google Scholar 

  • Endo T, Ishida S, Ishikawa N and Sato F (2008) Chloroplastic NAD(P)H dehydrogenase complex and cyclic electron transport around Photosystem I. Mol Cells 25: 158–162

    PubMed  CAS  Google Scholar 

  • Finel M (1998) Does NADH play a central role in energy metabolism in Helicobacter pylori? Trends Biochem Sci 23: 412–414

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T and Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its module common with membrane-bound multisubunit hydrogenases. FEBS Lett 479: 1–5

    Article  PubMed  CAS  Google Scholar 

  • Friedrich T, Steinmüller K and Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 367: 107–111

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto M, Endo T, Peltier G, Tasaka M and Shikanai T (2003) A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J 36: 541–549

    Article  PubMed  CAS  Google Scholar 

  • Heazlewood JL, Howell KA and Millar AH (2003) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant-specific subunits. Biochim Biophys Acta 1604: 159–169

    Article  PubMed  CAS  Google Scholar 

  • Herranen M, Battchikova N, Zhang P, Graf A, Sirpiö S, Paakkarinen V and Aro E-M (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134: 470–481

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Howitt CA, Smith GD and Day DA (1993) Cyanide-insensitive oxygen uptake and pyridine nucleotide dehydrogenases in the cyanobacterium Anabaena PCC 7120. Biochim Biophys Acta 1141: 313–320

    Article  CAS  Google Scholar 

  • Howitt C, Udall PK and Vermaas W (1999) Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. J Bacteriol 181: 3994–4003

    PubMed  CAS  Google Scholar 

  • Ishida S, Takabayashi A, Ishikawa N, Hano Y, Endo T and Sato F (2009) A novel nuclear-encoded protein, NDH-dependent cyclic electron flow 5, is essential for the accumulation of chloroplast NAD(P)H dehydrogenase complexes. Plant Cell Physiol 50: 383–393

    Article  PubMed  CAS  Google Scholar 

  • Ishihara S, Takabayashi A, Ido K, Endo T, Ifuku K and Sato F (2007) Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol 145: 668–679

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa N, Takabayashi A, Ishida S, Endo T and Sato F (2008) NDF6: a thylakoid protein specific to terrestrial plants is essential for activity of chloroplastic NAD(P)H dehydrogenase in Arabidopsis. Plant Cell Physiol 49: 1066–1073

    Article  PubMed  CAS  Google Scholar 

  • Joët T, Cournac L, Peltier G and Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128: 760–769

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A and Reinhold L (1999) The CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539–570

    Article  PubMed  CAS  Google Scholar 

  • Kaplan A, Hagemann M, Bauwe H, Kahlon S and Ogawa T (2007) Carbon acquisition by cyanobacteria: mechanisms, comparative genomics, and evolution. In: Herrero A and Flores E (eds) The Cyanobacteria: Molecular Biology, Genomics and Evolution, pp 305–334. Horizon Scientific Press, Norwich, UK

    Google Scholar 

  • Klughammer B, Sültemeyer D, Badger MR and Price GD (1999) The involvement of NAD(P)H dehydrogenase subunits, NdhD3 and NdhF3, in high-affinity CO2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol Microbiol 32: 1305–1315

    Article  PubMed  CAS  Google Scholar 

  • Kuntz M (2004) Plastid terminal oxidase and its biological significance. Planta 218: 896–899

    Article  PubMed  CAS  Google Scholar 

  • Ma W and Mi H (2008) Effect of exogenous glucose on the expression and activity of NADPH dehydrogenase complexes in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol Biochem 46: 775–779

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Deng Y, Ogawa T and Mi H (2006) Active NDH-1 complexes from the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol 47: 1432–1436

    Article  PubMed  CAS  Google Scholar 

  • Maeda S, Badger MR and Price GD (2002) Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43: 425–435

    Article  PubMed  CAS  Google Scholar 

  • Majeran W, Zybailov B, Ytterberg AJ, Dunsmore J, Sun Q and van Wijk KJ (2008) Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Mol Cell Proteomics 7: 1609–1638

    Article  PubMed  CAS  Google Scholar 

  • Marco E, Ohad N, Schwarz R, Lieman-Hurwitz J, Gabay C and Kaplan A (1993) High CO2 concentration alleviates the block in photosynthetic electron transport in an ndhB-inactivated mutant of Synechococcus sp. PCC 7942. Plant Physiol 101: 1047–1053

    Article  PubMed  CAS  Google Scholar 

  • Mathiesen C and Hägerhäll C (2003) The ‘antiporter module’ of respiratory chain complex I includes the MrpC/NuoK subunit—a revision of the modular evolution scheme. FEBS Lett 549: 7–13

    Article  PubMed  CAS  Google Scholar 

  • Matsuo M, Endo T and Asada K (1998a) Properties of the respiratory NAD(P)H dehydrogenase isolated from the cyanobacterium Synechocystis PCC6803. Plant Cell Physiol 39: 263–267

    Article  CAS  Google Scholar 

  • Matsuo M, Endo T and Asada K (1998b) Isolation of a novel NAD(P)H-quinone oxidoreductase from the cyanobacterium synechocystis PCC6803. Plant Cell Physiol 39: 751–755

    Article  CAS  Google Scholar 

  • McDonald AE and Vanlerberghe GC (2006) Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp Biochem Biophys Part D1: 357–364

    Google Scholar 

  • Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992a) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33: 1233–1237

    CAS  Google Scholar 

  • Mi H, Endo T, Schreiber U and Asada K (1992b) Donation of electrons from cytosolic components to the intersystem chain in the cyanobacterium Synechococcus sp. PCC 7002 as determined by reduction of P700+. Plant Cell Physiol 33: 1099–1105

    CAS  Google Scholar 

  • Mi H, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661–668

    CAS  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M and 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, Miyake C, Tomizawa K, Endo T, Tasaka M and Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429: 579–582

    Article  PubMed  CAS  Google Scholar 

  • Munshi MK, Kobayashi Y and Shikanai T (2005) Identification of a novel protein, CRR7, required for the stabilization of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant J 44: 1036–1044

    Article  CAS  Google Scholar 

  • Munshi MK, Kobayashi Y and Shikanai T (2006) CHLORORESPIRATORY REDUCTION 6 is a novel factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiol 141: 737–744

    Article  PubMed  CAS  Google Scholar 

  • Muraoka R, Okuda K, Kobayashi Y and Shikanai T (2006) A eukaryotic factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiol 142: 1683–1689

    Article  PubMed  CAS  Google Scholar 

  • Nixon PJ and Mullineaux CW (2001) Regulation of photosynthetic electron transport. In: Aro E-M and Andersson B (eds) Regulation of Photosynthesis. Advances in Photosynthesis and Respiration, vol 11, pp 533–555. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Nixon PJ and Rich PR (2006) Chlororespiratory pathways and their physiological significance. In: Wise RR and Hoober JK (eds) The Structure and Function of Plastids. Advances in Photosynthesis and Respiration, vol 23, pp 237–251. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Chapter  Google Scholar 

  • Norling B, Zak E, Andersson B and Pakrasi H (1998) 2D-isolation of pure plasma and thylakoid membranes from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 436: 189–192

    Article  PubMed  CAS  Google Scholar 

  • Nowaczyk MM, Wulfhorst H, Ryan CM, Souda P, Zhang H, Cramer WA and Whitelegge JP (2011) NdhP and NdhQ: Two novel small subunits of the cyanobacterial NDH-1 complex. Biochemistry

    Google Scholar 

  • Ogawa T (1991a) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc Natl Acad Sci USA 88: 4275–4279

    Article  CAS  Google Scholar 

  • Ogawa T (1991b) Cloning and inactivation of a gene essential to inorganic carbon transport of Synechocystis PCC6803. Plant Physiol 96: 280–284

    Article  CAS  Google Scholar 

  • Ogawa T (1992) Identification and characterization of the ictA/ndhL gene product essential to inorganic carbon transport of Synechocystis sp. strain PCC6803. Plant Physiol 99: 1604–1608

    Article  PubMed  CAS  Google Scholar 

  • Ogawa T and Mi H (2007) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93: 69–77

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Katoh H and Ogawa T (1998) The use of mutants in the analysis of the CO2-concentrating mechanism in cyanobacteria. Can J Bot 76: 1035–1042

    CAS  Google Scholar 

  • Ohkawa H, Pakrasi HB and Ogawa T (2000a) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC 6803. J Biol Chem 275: 31630–31634

    Article  CAS  Google Scholar 

  • Ohkawa H, Price GD, Badger MR and Ogawa T (2000b) Mutation of ndh genes leads to inhibition of CO2 uptake rather than HCO3 uptake in Synechocystis sp. strain PCC 6803. J Bacteriol 182: 2591–2596

    Article  CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Shibata M and Ogawa T (2001) Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183: 4938–4939

    Article  PubMed  CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Hagino N, Shibata M, Pakrasi HB and Ogawa T (2002) Functionally distinct NAD(P)H dehydrogenases and their membrane localization in Synechocystis sp. PCC6803. Funct Plant Biol 29: 195–200

    Article  CAS  Google Scholar 

  • Omata T and Ogawa T (1985) Changes in the polypeptide composition of the cytoplasmic membrane in the cyanobacterium Anacystis nidulans during adaptation to low CO2 conditions. Plant Cell Physiol 26: 1075–1081

    CAS  Google Scholar 

  • Omata T, Price GD, Badger MR, Okamura M, Gohta S and Ogawa T (1999) Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96: 13571–13576

    Article  PubMed  CAS  Google Scholar 

  • Pasquier C and Hamodrakas SJ (1999) An hierarchical artificial neural network system for the classification of transmembrane proteins. Protein Eng 12: 631–634

    Article  PubMed  CAS  Google Scholar 

  • Peltier G and Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53: 523–550

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Shimizu H and Shikanai T (2008) The chloroplast NAD(P)H dehydrogenase complex interacts with Photosystem I in Arabidopsis. J Biol Chem 283: 34873–34879

    Article  PubMed  CAS  Google Scholar 

  • Peschek GA (1980) Electron transport reactions in respiratory particles of hydrogenase-induced Anacystis nidulans. Arch Microbiol 125: 123–131

    Article  CAS  Google Scholar 

  • Pieulle L, Guedeney G, Cassier-Chauvat C, Jeanjean R, Chauvat F and Peltier G (2000) The gene encoding the NdhH subunit of type 1 NAD(P)H dehydrogenase is essential to survival of Synechocystis PCC6803. FEBS Lett 487: 272–276

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Sültemeyer D, Klughammer B, Ludwig M and Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can J Bot 76: 973–1002

    CAS  Google Scholar 

  • Price GD, Maeda S, Omata T and Badger MR (2002) Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. Funct Plant Biol 29: 131–149

    Article  CAS  Google Scholar 

  • Price GD, Woodger FJ, Badger MR, Howitt SM and Tucker L (2004) Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101: 18228–18233

    Article  PubMed  CAS  Google Scholar 

  • Price GD, Badger MR, Woodger FJ and Long BM (2008) Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441–1461

    Article  PubMed  CAS  Google Scholar 

  • Prommeenate P, Lennon AM, Markert C, Hippler M and Nixon PJ (2004) Subunit composition of NDH-1 complexes of Synechocystis sp. PCC 6803: identification of two new ndh gene products with nuclear-encoded homologues in the chloroplast Ndh complex. J Biol Chem 279: 28165–28173

    Article  PubMed  CAS  Google Scholar 

  • Rumeau D, Becuwe-Linka N, Beyly A, Louwagie M, Garin J and Peltier G (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17: 219–232

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sazanov LA (2007) Respiratory complex I: mechanistic and structural insights provided by the crystal structure of the hydrophilic domain. Biochemistry 46: 2275–2288

    Article  PubMed  CAS  Google Scholar 

  • Sazanov LA and Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311: 1430–1436

    Article  PubMed  CAS  Google Scholar 

  • Sazanov LA, Burrows PA and Nixon PJ (1998) The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue of from pea thylakoid membranes. Proc Natl Acad Sci USA 95: 1319–1324

    Article  PubMed  CAS  Google Scholar 

  • Scherer S, Almon H and Böger P (1988) Interaction of photosynthesis, respiration and nitrogen fixation in cyanobacteria. Photosynth Res 15: 95–114

    Article  CAS  Google Scholar 

  • Schluchter WM, Zhao J and Bryant DA (1993) Isolation and characterization of the ndhF gene of Synechococcus sp. strain PCC 7002 and initial characterization of an interposon mutant. J Bacteriol 175: 3343–3352

    PubMed  CAS  Google Scholar 

  • Schmetterer G (1994) Cyanobacterial respiration. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria. Advances in Photosynthesis and Respiration, vol 1, pp 409–435. Springer, Dordrecht, The Netherlands

    Chapter  Google Scholar 

  • Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A and Ogawa T (2001) Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98: 11789–11794

    Article  PubMed  CAS  Google Scholar 

  • Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H, Kaplan A and Ogawa T (2002a) Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: function and phylogenetic analysis. J Biol Chem 277: 18658–18664

    Article  CAS  Google Scholar 

  • Shibata M, Ohkawa H, Katoh H, Shimoyama M and Ogawa T (2002b) Two CO2 uptake systems in cyanobacteria: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC 6803. Funct Plant Biol 29: 123–129

    Article  CAS  Google Scholar 

  • Shikanai T and Endo T (2000) Physiological function of a respiratory complex, NAD(P)H dehydrogenase in chloroplasts: dissection by chloroplast reverse genetics. Plant Biotech 17: 79–86

    Article  CAS  Google Scholar 

  • Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K and Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95: 9705–9709

    Article  PubMed  CAS  Google Scholar 

  • Shimizu H and Shikanai T (2007) Dihydrodipicolinate reductase-like protein, CRR1, is essential for chloroplast NAD(P)H dehydrogenase in Arabidopsis. Plant J 52: 539–547

    Article  PubMed  CAS  Google Scholar 

  • Shimizu H, Peng L, Myouga F, Motohashi R, Shinozaki K and Shikanai T (2008) CRR23/NdhL is a Subunit of the Chloroplast NAD(P)H Dehydrogenase Complex in Arabidopsis. Plant Cell Physiol 49: 835–842

    Article  PubMed  CAS  Google Scholar 

  • Sirpiö S, Allahverdiyeva Y, Holmstrom M, Khrouchtchova A, Haldrup A, Battchikova N and Aro E-M (2009) Novel nuclear-encoded subunits of the chloroplast NAD(P)H dehydrogenase complex. J Biol Chem 284: 905–912

    Article  PubMed  CAS  Google Scholar 

  • Takabayashi A, Ishikawa N, Obayashi T, Ishida S, Obokata J, Endo T and Sato F (2009) Three novel subunits of Arabidopsis chloroplastic NAD(P)H dehydrogenase identified by bioinformatic and reverse genetic approaches. Plant J 57: 207–219

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Katada S, Ishikawa H, Ogawa T and Takabe T (1997) Electron flow from NAD(P)H dehydrogenase to photosystem I is required for adaptation to salt shock in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 38: 1311–1318

    Article  CAS  Google Scholar 

  • Tchernov D, Helman Y, Keren N, Luz B, Ohad I, Reinhold L, Ogawa T and Kaplan A (2001) Passive entry of CO2 and its energy-dependent intracellular conversion to HCO3 in cyanobacteria are driven by a photosystem I-generated ΔμH+. J Biol Chem 276: 23450–23455

    Article  PubMed  CAS  Google Scholar 

  • Volokita M, Zenvirth D, Kaplan A and Reinhold L (1984) Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol 76: 599–602

    Article  PubMed  CAS  Google Scholar 

  • Wang H-L, Postier BL and Burnap RL (2004) Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem 279: 5739–5751

    Article  PubMed  CAS  Google Scholar 

  • Wastyn M, Achatz A, Molitor V and Peschek GA (1988) Respiratory activities and aa 3-type cytochrome oxidase in plasma and thylakoid membranes from vegetative cells and heterocysts of the cyanobacterium Anabaena ATCC 29413. Biochim Biophys Acta 935: 217–224

    Article  CAS  Google Scholar 

  • Weerakoon DR and Olson JW (2008) The Campylobacter jejuni NADH:ubiquinone oxidoreductase (Complex I) utilizes flavodoxin rather than NADH. J Bacteriol 190: 915–925

    Article  PubMed  CAS  Google Scholar 

  • Weidner U, Geier S, Ptock A, Friedrich T, Leif H and Weiss H (1993) The gene locus of the proton-translocating NADH:ubiquinone oxidoreductase in Escherichia coli. J Mol Biol 233: 109–122

    Article  PubMed  CAS  Google Scholar 

  • Xu M, Ogawa T, Pakrasi HB and Mi H (2008) Identification and Localization of the CupB Protein Involved in Constitutive CO2 Uptake in the Cyanobacterium, Synechocystis sp. Strain PCC 6803. Plant Cell Physiol 49: 994–997

    Article  PubMed  CAS  Google Scholar 

  • Yagi T, Yano T, Di Bernardo S and Matsuno-Yagi A (1998) Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1364: 125–133

    Article  PubMed  CAS  Google Scholar 

  • Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ, Vermaas WFJ, Havaux M and 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, Battchikova N, Jansen T, Appel J, Ogawa T and Aro E-M (2004) Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803. Plant Cell 16: 3326–3340

    Article  PubMed  CAS  Google Scholar 

  • Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi HB, Ogawa T and Aro E-M (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390: 513–520

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

PJN is grateful to the Biotechnology and Biological Sciences Research Council for financial support. EMA acknowledges the Academy of Finland (Project No. 118637), the EU project Solar-H2 (FP7 contract no 212508), Nordic Energy and the Maj and Tor Nessling Foundation for support of research.

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Correspondence to Peter J. Nixon .

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Battchikova, N., Aro, EM., Nixon, P.J. (2011). Structure and Physiological Function of NDH-1 Complexes in Cyanobacteria. In: Peschek, G., Obinger, C., Renger, G. (eds) Bioenergetic Processes of Cyanobacteria. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0388-9_16

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