Advertisement

Photosynthesis Research

, Volume 126, Issue 2–3, pp 341–349 | Cite as

NDH-1L interacts with ferredoxin via the subunit NdhS in Thermosynechococcus elongatus

  • Zhihui He
  • Fangfang Zheng
  • Yaozong Wu
  • Qinghua Li
  • Jing Lv
  • Pengcheng Fu
  • Hualing Mi
Regular Paper

Abstract

The large size complex of cyanobacterial NAD(P)H dehydrogenase (NDH-1) complex (NDH-1L) plays crucial role in a variety of bioenergetic reactions such as respiration and cyclic electron flow around photosystem I. Although the complex has been isolated and identified, its biochemical function still remains to be clarified. Here, we highly purified the NDH-1L complex from the cells of Thermosynechococcus elongatus by Ni2+ affinity chromatography and size-exclusion chromatography. The purified NDH-1L complex has an apparent total molecular mass of approximately 500 kDa. 14 known subunits were identified by mass spectrometry and immunoblotting, including the NdhS subunit containing ferredoxin (Fd)-docking site domain. Surface plasmon resonance measurement demonstrates that the NDH-1L complex could bind to Fd with the binding constant (K D) of 59 µM. Yeast two-hybrid system assay further confirmed the interaction of Fd with NdhS and indicated that NdhH is involved in the interaction. Our results provide direct biochemical evidence that the cyanobacterial NDH-1 complex catalyzes the electron transport from reduced Fd to plastoquinone via NdhS and NdhH.

Keywords

Cyanobacteria NDH-1 complex Purification Ferredoxin Surface plasmon resonance Thermosynechococcus elongatus 

Abbreviations

BisTris

2-Bis(2-hydroxyethyl)amino-2-(hydroxymethyl)-1,3-propanediol

BN

Blue native

DDM

n-Dodecyl-β-d-maltoside

Fd

Ferredoxin

FNR

Fd:NADP+ oxidoreductase

NDH-1

Type-1 NAD(P)H dehydrogenase

NDH-1L

Large size NDH-1 complex

PQ

Plastoquinone

PSI

Photosystem I

SH3

Src homology 3

SPR

Surface plasmon resonance

Synechocystis 6803

Synechocystis sp. PCC 6803

T. elongatus

Thermosynechococcus elongatus

Notes

Acknowledgments

This work was supported by funds from the State Key Basic Research and Development Plant 973 [2015CB150104, 2013CB127005, 2011C13200902] and the National Natural Science Foundation of China [31270286] and Shanghai Science Foundation [13DJ1400102] to H. Mi.

Supplementary material

11120_2015_90_MOESM1_ESM.docx (17 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Battchikova N, Zhang P, Rudd S, Ogawa T, Aro E-M (2005) Identification of NdhL and Ssl1690 (NdhO) in NDH-1L and NDH-1M complexes of Synechocystis sp. PCC 6803. J Biol Chem 280(4):2587–2595CrossRefPubMedGoogle Scholar
  2. Battchikova N, Eisenhut M, Aro E-M (2011a) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944CrossRefPubMedGoogle Scholar
  3. Battchikova N, Wei L, Du L, Bersanini L, Aro E-M, Ma W (2011b) Identification of a novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. J Biol Chem 286(42):36992–37001PubMedCentralCrossRefPubMedGoogle Scholar
  4. Berger S, Ellersiek U, Kinzelt D, Steinmiiller K (1993) Immunopurification of a subcomplex of the NAD(P)H-plastoquinone-oxidoreductase from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 326:246–250CrossRefPubMedGoogle Scholar
  5. Birungi M, Folea M, Battchikova N, Xu M, Mi H, Ogawa T, Aro E-M, Boekema EJ (2010) Possibilities of subunit localization with fluorescent protein tags and electron microscopy exemplified by a cyanobacterial NDH-1 study. Biochim Biophys Acta 1797(9):1681–1686CrossRefPubMedGoogle Scholar
  6. Deng Y, Ye JY, Mi H, Shen YG (2003) Separation of hydrophobic NAD(P)H dehydrogenase subcomplexes from cyanobacterium Synechocystis PCC 6803. Acta Biochim Biophys Sin 35(8):723–727PubMedGoogle Scholar
  7. Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465(7297):441–445CrossRefPubMedGoogle Scholar
  8. Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and its MOD common with membrane-bound multisubunit hydrogenases. FEBS Lett 479(1–2):1–5CrossRefPubMedGoogle Scholar
  9. Friedrich T, Steinmüller K, Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 367(2):107–111CrossRefPubMedGoogle Scholar
  10. Herranen M, Battchikova N, Zhang P, Graf A, Sirpio S, Paakkarinen V, Aro E-M (2004) Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol 134(1):470–481PubMedCentralCrossRefPubMedGoogle Scholar
  11. Hu P, Lv J, Fu P, Mi H (2013) Enzymatic characterization of an active NDH complex from Thermosynechococcus elongatus. FEBS Lett 587(15):2340–2345CrossRefPubMedGoogle Scholar
  12. Jonsson U, Fagerstam L, Ivarsson B, Johnsson B, Karlsson R, Lundh K, Lofas S, Persson B, Roos H, Ronnberg I (1991) Real-time biospecific interaction analysis using surface plasmon resonance and a sensor chip technology. Biotechniques 11(5):620–627PubMedGoogle Scholar
  13. Klughammer B, Sültemeyer D, Badger MR, 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(6):1305–1315CrossRefPubMedGoogle Scholar
  14. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685CrossRefPubMedGoogle Scholar
  15. Ma W, 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(8–9):775–779CrossRefPubMedGoogle Scholar
  16. Ma W, Deng Y, Ogawa T, Mi H (2006) Active NDH-1 complexes from the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Cell Physiol 47(10):1432–1436CrossRefPubMedGoogle Scholar
  17. Matsuo M, Endo T, Asada K (1998) Properties of the respiratory NAD(P)H dehydrogenase isolated from the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 39(3):263–267CrossRefPubMedGoogle Scholar
  18. Mi H, Endo T, Schreiber U, Ogawa T, Asada K (1992) 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(8):1233–1237Google Scholar
  19. Mi H, Endo T, Ogawa T, 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(4):661–668Google Scholar
  20. Munekage Y, Hashimoto M, Miyake C, Tomizawa K-I, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429(6991):579–582CrossRefPubMedGoogle Scholar
  21. Nowaczyk MM, Wulfhorst H, Ryan CM, Souda P, Zhang H, Cramer WA, Whitelegge JP (2011) NdhP and NdhQ: two novel small subunits of the cyanobacterial NDH-1 complex. Biochemistry 50(7):1121–1124PubMedCentralCrossRefPubMedGoogle Scholar
  22. Ogawa T (1991) 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(10):4275–4279PubMedCentralCrossRefPubMedGoogle Scholar
  23. Ogawa T, Mi H (2007 ) Cyanobacterial NADPH dehydrogenase complexes. Photosynth Res 93(1–3):69–77CrossRefPubMedGoogle Scholar
  24. Ohkawa H, Pakrasi HB, Ogawa T (2000) Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC 6803. J Biol Chem 275(41):31630–31634CrossRefPubMedGoogle Scholar
  25. Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53(1):523–550CrossRefPubMedGoogle Scholar
  26. Prommeenate P, Lennon AM, Markert C, Hippler M, 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(27):28165–28173CrossRefPubMedGoogle Scholar
  27. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311(5766):1430–1436CrossRefPubMedGoogle Scholar
  28. Sazanov LA, Burrows PA, Nixon PJ (1998) The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. Proc Natl Acad Sci USA 95(3):1319–1324PubMedCentralCrossRefPubMedGoogle Scholar
  29. Schwarz D, Schubert H, Georg J, Hess WR, Hagemann M (2013) The gene sml0013 of Synechocystis species strain PCC 6803 encodes for a novel subunit of the NAD(P)H oxidoreductase or complex I that is ubiquitously distributed among cyanobacteria. Plant Physiol 163(3):1191–1202PubMedCentralCrossRefPubMedGoogle Scholar
  30. Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, Kaplan A, 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(20):11789–11794PubMedCentralCrossRefPubMedGoogle Scholar
  31. Webber A, Wulfhorst H, Franken LE, Wessinghage T, Boekema EJ, Nowaczyk MM (2014) The 5 kDa protein NdhP is essential for stable NDH-1L assembly in Thermosynechococcus elongatus. PLoS One 9(8):e103584CrossRefGoogle Scholar
  32. Xu M, Ogawa T, Pakrasi HB, 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(6):994–997CrossRefPubMedGoogle Scholar
  33. Yamamoto H, Shikanai T (2013) In Planta mutagenesis of Src homology 3 domain-like fold of NdhS, a ferredoxin-binding subunit of the chloroplast NADH dehydrogenase-like complex in Arabidopsis: a conserved Arg-193 plays a critical role in ferredoxin binding. J Biol Chem 288(51):36328–36337PubMedCentralCrossRefPubMedGoogle Scholar
  34. Yamamoto H, Peng L, Fukao Y, Shikanai T (2011) An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23(4):1480–1493PubMedCentralCrossRefPubMedGoogle Scholar
  35. Zhang P, Battchikova N, Jansen T, Appel J, Ogawa T, 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(12):3326–3340PubMedCentralCrossRefPubMedGoogle Scholar
  36. Zhang P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi Himadri B, Ogawa T, Aro E-M (2005) Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. Biochem J 390(2):513–520PubMedCentralCrossRefPubMedGoogle Scholar
  37. Zhang M, Li G, Huang W, Bi T, Chen G, Tang Z, Su W, Sun W (2010) Proteomic study of Carissa spinarum in response to combined heat and drought stress. Proteomics 10(17):3117–3129CrossRefPubMedGoogle Scholar
  38. Zhang J, Gao F, Zhao J, Ogawa T, Wang Q, Ma W (2014) NdhP is an exclusive subunit of large complex of NADPH dehydrogenase essential to stabilize the complex in Synechocystis sp. strain PCC 6803. J Biol Chem 289(27):18770–18781PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Zhihui He
    • 1
  • Fangfang Zheng
    • 1
  • Yaozong Wu
    • 1
  • Qinghua Li
    • 1
  • Jing Lv
    • 2
  • Pengcheng Fu
    • 2
  • Hualing Mi
    • 1
  1. 1.National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological SciencesChinese Academy of ScienceShanghaiChina
  2. 2.Renewable Energy Research CenterChina University of Petroleum BeijingBeijingChina

Personalised recommendations