Skip to main content
SpringerLink
Log in

Cyanobacterial NDH-1-Photosystem I Supercomplex

  • Chapter
  • First Online:
Microbial Photosynthesis

  • 1154 Accesses

Abstract

Cyanobacterial NDH-1-photosystem I (PSI) supercomplex is localized in the thylakoid membrane, and its formation facilitates cyclic electron transfer around PSI (PSI CET) via NDH-1. Similar NDH-1-PSI supercomplex has also been identified in the majority of higher plants, but not in liverwort. We describe in this book chapter the cyanobacterial NDH-1-PSI supercomplex, focusing on its identification, function, assembly, and evolution from cyanobacteria to higher plants.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

CpcG2-PBS:

CpcG2-phycobilisome

Fd:

ferredoxin

NAI130:

an NDH-1 hydrophilic arm assembly intermediate complex with molecular mass of about 130 kDa

NAI300:

an NDH-1 hydrophilic arm assembly intermediate complex with molecular mass of about 300 kDa

NDH-CET:

NDH-1-mediated cyclic electron transfer around photosystem I

OPS:

oxygenic photosynthesis-specific

PSI CET:

cyclic electron transport around photosystem I

Synechocystis 6803:

Synechocystis sp. strain PCC 6803

References

  • Alboresi, A., Caffarri, S., Nogue, F., Bassi, R., & Morosinotto, T. (2008). In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: Identification of subunits which evolved upon land adaptation. PLoS One, 3, e2033.

    PubMed  PubMed Central  Google Scholar 

  • Armbruster, U., Rühle, T., Kreller, R., Strotbek, C., Zühlke, J., Tadini, L., Blunder, T., Hertle, A. P., Qi, Y., Rengstl, B., Nickelsen, J., Frank, W., & Leister, D. (2013). The photosynthesis affected mutant68-like protein evolved from a PSII assembly factor to mediate assembly of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell, 25, 3926–3943.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arnon, D. I. (1971). The light reactions of photosynthesis. Proceedings of the National Academy of Sciences of the United States of America, 68, 2883–2892.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Arteni, A. A., Zhang, P., Battchikova, N., Ogawa, T., Aro, E. M., & Boekema, E. J. (2006). Structural characterization of NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochimica et Biophysica Acta, 1757, 1469–1475.

    CAS  PubMed  Google Scholar 

  • Battchikova, N., & Aro, E. M. (2007). Cyanobacterial NDH-1 complexes: Multiplicity in function and subunit composition. Physiologia Plantarum, 131, 22–32.

    CAS  PubMed  Google Scholar 

  • 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. The Journal of Biological Chemistry, 280, 2587–2595.

    CAS  PubMed  Google Scholar 

  • Battchikova, N., Wei, L., Du, L., Bersanini, L., Aro, E. M., & Ma, W. (2011a). 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. The Journal of Biological Chemistry, 286, 36992–37001.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Battchikova, N., Eisenhut, M., & Aro, E. M. (2011b). Cyanobacterial NDH-1 complexes: Novel insights and remaining puzzles. Biochimica et Biophysica Acta, 1807, 935–944.

    CAS  PubMed  Google Scholar 

  • Bernát, G., Appel, J., Ogawa, T., & Rögner, M. (2011). Distinct roles of multiple NDH-1 complexes in the cyanobacterial electron transport network as revealed by kinetic analysis of P700+ reduction in various ndh-deficient mutants of Synechocystis sp. strain PCC6803. Journal of Bacteriology, 193, 292–295.

    PubMed  Google Scholar 

  • Dai, H., Zhang, L., Zhang, J., Mi, H., Ogawa, T., & Ma, W. (2013). Identification of a cyanobacterial CRR6 protein, Slr1097, required for efficient assembly of NDH-1 complexes in Synechocystis sp. PCC 6803. The Plant Journal, 75, 858–866.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gao, F., Zhao, J., Wang, X., Qin, S., Wei, L., & Ma, W. (2016a). NdhV is a subunit of NADPH dehydrogenase essential for cyclic electron transport in Synechocystis sp. strain PCC 6803. Plant Physiology, 170, 752–760.

    CAS  PubMed  Google Scholar 

  • Gao, F., Zhao, J., Chen, L., Battchikova, N., Ran, Z., Aro, E. M., Ogawa, T., & Ma, W. (2016b). The NDH-1L-PSI supercomplex is important for efficient cyclic electron transport in cyanobacteria. Plant Physiology, 172, 1451–1464.

    CAS  PubMed  PubMed Central  Google Scholar 

  • He, Z., & Mi, H. (2016). Functional characterization of the subunits N, H, J, and O of the NAD(P)H dehydrogenase complexes in Synechocystis sp. strain PCC 6803. Plant Physiology, 171, 1320–1332.

    Google Scholar 

  • He, Z., Xu, M., Wu, Y., Lv, J., Fu, P., & Mi, H. (2016). NdhM subunit is required for the stability and the function of NAD(P)H dehydrogenase complexes involved in CO2 uptake in Synechocystis sp. strain PCC 6803. The Journal of Biological Chemistry, 291, 5902–5912.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A., & Ikeuchi, M. (2001). DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell, 13, 793–806.

    CAS  PubMed  PubMed Central  Google Scholar 

  • KouÅ™il, R., Strouhal, O., Nosek, L., Lenobel, R., Chamrád, I., Boekema, E. J., Å ebela, M., & Ilík, P. (2014). Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. The Plant Journal, 77, 568–576.

    PubMed  Google Scholar 

  • Kramer, D. M., & Evans, J. R. (2011). The importance of energy balance in improving photosynthetic productivity. Plant Physiology, 155, 70–78.

    CAS  PubMed  Google Scholar 

  • Laughlin, T. G., Bayne, A. N., Trempe, J. F., Savage, D. F., & Davies, K. M. (2019). Structure of the complex I-like molecule NDH of oxygenic photosynthesis. Nature, 566, 411–414.

    PubMed  Google Scholar 

  • Ma, W., & Ogawa, T. (2015). Oxygenic photosynthesis-specific subunits of cyanobacterial NADPH dehydrogenases. IUBMB Life, 67, 3–8.

    CAS  PubMed  Google Scholar 

  • 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 Physiology, 33, 1233–1237.

    CAS  Google Scholar 

  • Neilson, J. A. D., & Durnford, D. G. (2010). Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynthesis Research, 106, 57–71.

    CAS  PubMed  Google Scholar 

  • Ogawa, T. (1991). A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC 6803. Proceedings of the National Academy of Sciences of the United States of America, 88, 4275–4279.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ohkawa, H., Pakrasi, H. B., & Ogawa, T. (2000). Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC6803. The Journal of Biological Chemistry, 275, 31630–31634.

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Pan, X., Cao, D., Xie, F., Xu, F., Su, X., Mi, H., Zhang, X, & Li, M. (2020). Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nature Communications, 11, 610. 

    Google Scholar 

  • Peltier, G., Aro, E. M., & Shikanai, T. (2016). NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annual Review of Plant Biology, 67, 55–80.

    CAS  PubMed  Google Scholar 

  • Peng, L., Shimizu, H., & Shikanai, T. (2008). The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. The Journal of Biological Chemistry, 283, 34873–34879.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, L., Fukao, Y., Fujiwara, M., Takami, T., & Shikanai, T. (2009). Efficient operation of NAD(P)H dehydrogenase requires the supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell, 21, 3623–3640.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, L., Fukao, Y., Fujiwara, M., & Shikanai, T. (2012). Multistep assembly of chloroplast NADH dehydrogenase-like subcomplex A requires several nucleus-encoded proteins, including CRR41 and CRR42, in Arabidopsis. Plant Cell, 24, 202–214.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prommeenate, P., Lennon, A. M., Markert, C., Hippler, M., & Nixon, P. J. (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. The Journal of Biological Chemistry, 279, 28165–28173.

    CAS  PubMed  Google Scholar 

  • Ran, Z., Zhao, J., Tong, G., Gao, F., Wei, L., & Ma, W. (2019). Ssl3451 is important for accumulation of NDH-1 assembly intermediates in the cytoplasm of Synechocystis sp. strain PCC 6803. Plant & Cell Physiology, 60, 1374–1385.

    CAS  Google Scholar 

  • Schuller, J. M., Birrell, J. A., Tanaka, H., Konuma, T., Wulfhorst, H., Cox, N., Schuller, S. K., Thiemann, J., Lubitz, W., Sétif, P., Ikegami, T., Engel, B. D., Kurisu, G., & Nowaczyk, M. M. (2019). Structural adaptations of photosynthetic complex I enable ferredoxin-dependent electron transfer. Science, 363, 257–260.

    CAS  PubMed  Google Scholar 

  • 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. Proceedings of the National Academy of Sciences of the United States of America, 98, 11789–11794.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ueda, M., Kuniyoshi, T., Yamamoto, H., Sugimoto, K., Ishizaki, K., Kohchi, T., Nishimura, Y., & Shikanai, T. (2012). Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. The Plant Journal, 72, 683–693.

    CAS  PubMed  Google Scholar 

  • Wang, X., Gao, F., Zhang, J., Zhao, J., Ogawa, T., & Ma, W. (2016). A cytoplasmic protein Ssl3829 is important for NDH-1 hydrophilic arm assembly in Synechocystis sp. strain PCC 6803. Plant Physiology, 171, 864–877.

    Google Scholar 

  • Wulfhorst, H., Franken, L. E., Wessinghage, T., Boekema, E. J., & Nowaczyk, M. M. (2014). The 5 kDa protein NdhP is essential for stable NDH-1L assembly in Thermosynechococcus elongatus. PLoS One, 9, e103584.

    PubMed  PubMed Central  Google Scholar 

  • Xu, M., Ogawa, T., Pakrasi, H. B., & 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 Physiology, 49, 994–997.

    Google Scholar 

  • 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. The Journal of Biological Chemistry, 288, 36328–36337.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 1480–1493.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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, 3326–3340.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, C., Shuai, J., Ran, Z., Zhao, J., Wu, Z., Liao, R., Wu, J., Ma, W., & Lei, M. (2020). Structural insights into NDH-1 mediated cyclic electron transfer. Nature Communications, 11, 888.

    Google Scholar 

  • Zhao, J., Gao, F., Zhang, J., Ogawa, T., & Ma, W. (2014). NdhO, a subunit of NADPH dehydrogenase, destabilizes medium size complex of the enzyme in Synechocystis sp. strain PCC 6803. The Journal of Biological Chemistry, 289, 26669–26676.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (31570235 and 31770259) and Science and Technology Commission of Shanghai Municipality (17070502900 and 18DZ2260500).

Author information

Authors and Affiliations

  1. Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai, China

    Weimin Ma

Authors
  1. Weimin Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Weimin Ma .

Editor information

Editors and Affiliations

  1. Key laboratory of Plant Stress Biology, State Key Laboratory of Cotton Biology, School of Life Sciences, Henan University, Kaifeng, Henan, China

    Qiang Wang

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ma, W. (2020). Cyanobacterial NDH-1-Photosystem I Supercomplex. In: Wang, Q. (eds) Microbial Photosynthesis. Springer, Singapore. https://doi.org/10.1007/978-981-15-3110-1_2

Download citation

Publish with us

Policies and ethics

Search

Navigation