Skip to main content

Higher Plant and Cyanobacterial Photosystem I: Connected Cytochrome Pathways

  • Chapter
  • First Online:
Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 41))

  • 1670 Accesses

Summary

Oxygenic photosynthesis is the principal converter of sunlight into chemical energy on earth. The conversion of solar energy is catalyzed by four multi-subunit membrane protein complexes: photosystem I (PSI), photosystem II (PSII), the cytochrome b6-f complex (cytb 6 f) and ATP-synthase (FOF1). These protein complexes are connected by soluble electron carriers that are vital not only for the proper function of ATP and NADPH production but also to render the system highly efficient in different organisms and various environments, some of which are quite harsh. While the main fabric of the membrane complexes is highly conserved, their surfaces and interaction with the soluble factors provide the specificity and fine regulation of the operating system. One of the prime examples for this phenomenon is the cyanobacterial photosynthetic electron transport chain that is situated alongside with respiratory complexes, yet it stays unique by virtue of the interacting soluble components. Cyanobacteria contain many different cytochromes that potentially can donate electrons to both PSI and cytochrome oxidase, yet the two systems can operate separately in a synchronous mode. The crystal structure determination of photosynthetic and respiratory protein complexes shed light on the various partial reactions and explains how they can function alongside each other.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

ALA:

5-aminolevulinic acid

Cyt c6:

Cytochrome C6

Fd:

Ferredoxin

NDH1:

NADH:ubiquinone oxidoreductase I

Pc:

Plastocyanin

PSI:

Photosystem I

PSII:

Photosystem II

PTOX:

Plastoquinol terminal

References

  • Alperovitch-Lavy A, Sharon I, Rohwer F, Aro EM, Glaser F, Milo R, Nelson N, Béjà O (2011) Reconstructing a puzzle: existence of cyanophages containing both photosystem-I and photosystem-II gene suites inferred from oceanic metagenomic datasets. Environ Microbiol 13:24–32

    Article  CAS  PubMed  Google Scholar 

  • Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98:10037–10041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber J (2008) Photosynthetic generation of oxygen. Philos Trans R Soc Lond Ser B Biol Sci 363:2665–2674

    Article  CAS  Google Scholar 

  • Battchikova N, Eisenhut M, Aro EM (2010) Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim Biophys Acta 1807:935–944

    Article  PubMed  Google Scholar 

  • Baymann F, Rappaport F, Joliot P, Kallas T (2001) Rapid electron transfer to photosystem I and unusual spectral features of cytochrome c6 in Synechococcus sp. PCC 7002 in vivo. Biochemistry 40:10570–10577

    Article  CAS  PubMed  Google Scholar 

  • Bendall DS, Howe CJ, Nisbet EG, Nisbet RE (2008) Photosynthetic and atmospheric evolution. Introduction. Philos Trans R Soc Lond B Biol Sci 363:2625–2628

    Article  PubMed  PubMed Central  Google Scholar 

  • Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635

    Article  CAS  PubMed  Google Scholar 

  • Bernroitner M, Tangl D, Lucini C, Furtmüller PG, Peschek GA, Obinger C (2009) Cyanobacterial cytochrome c M: probing its role as electron donor for Cu A of cytochrome c oxidase. Biochim Biophys Acta (BBA)-Bioenerg 1787:135–143

    Article  CAS  Google Scholar 

  • Bialek W, Nelson M, Tamiola K, Kallas T, Szczepaniak A (2008) Deeply branching c6-like cytochromes of cyanobacteria. Biochemistry 47:5515–5522

    Article  CAS  PubMed  Google Scholar 

  • Bibby TS, Mary I, Nield J, Partensky F, Barber J (2003) Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature 424:1051–1054

    Article  CAS  PubMed  Google Scholar 

  • Bottin H, Mathis P (1985) Interaction of plastocyanin with the photosystem I reaction center: a kinetic study by flash absorption spectroscopy. Biochemistry 24:6453–6460

    Article  CAS  Google Scholar 

  • Chance B, Lee CP, Mela L (1967) Control and conservation of energy in the cytochrome chain. Fed Proc 26:1341–1354

    CAS  PubMed  Google Scholar 

  • Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, West-Johnsrud L, Zettler ER (1992) Prochlorococcus marinus nov. gen. nov. sp.: a marine prokaryote containing divinylchlorophyll a and b. Arch Microbiol 157:297–300

    Article  CAS  Google Scholar 

  • Chitnis PR, Purvis D, Nelson N (1991) Molecular cloning and targeted mutagenesis of the gene psaF encoding subunit III of photosystem I from the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 266:20146–20151

    CAS  PubMed  Google Scholar 

  • Cho YS, Pakrasi HB, Whitmarsh J (2000) Cytochrome cM from synechocystis 6803. Detection in cells, expression in Escherichia coli, purification and physical characterization. Eur J Biochem 267:1068–1074

    Article  CAS  PubMed  Google Scholar 

  • De la Cerda B, Navarro JA, Hervás M, De la Rosa MA (1997) Changes in the reaction mechanism of electron transfer from plastocyanin to photosystem I in the cyanobacterium Synechocystis sp. PCC 6803 as induced by site-directed mutagenesis of the copper protein. Biochemistry 36:10125–10130

    Article  PubMed  Google Scholar 

  • De la Cerda B, Diaz-Quintana A, Navarro JA, Hervás M, De la Rosa MA (1999) Site-directed mutagenesis of cytochrome c6 from Synechocystis sp. PCC 6803. The heme protein possesses a negatively charged area that may be isofunctional with the acidic patch of plastocyanin. J Biol Chem 274:13292–13297

    Article  PubMed  Google Scholar 

  • Delosme R (1991) Electron transfer from cytochrome f to photosystem I in green algae. Photosynth Res 29:45–54

    CAS  PubMed  Google Scholar 

  • Dinsdale EA, Edwards RA, Hall D, Angly F, Breitbart M, Brulc JM, Furlan M, …, Rohwer F (2008) Functional metagenomic profiling of nine biomes. Nature 452:629–632

    Google Scholar 

  • Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, …, Hess WR (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci U S A 100:10020–10025

    Google Scholar 

  • Duran RV, Hervas M, De La Rosa MA, Navarro JA (2004) The efficient functioning of photosynthesis and respiration in Synechocystis sp. PCC 6803 strictly requires the presence of either cytochrome c6 or plastocyanin. J Biol Chem 279:7229–7233

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan HN, Cramer WA (1970) The redox potential of cytochromes b-559 and b-563 in spinach chloroplasts. Biochim Biophys Acta 216:200–207

    Article  CAS  PubMed  Google Scholar 

  • Farah J, Rappaport F, Choquet Y, Joliot P, Rochaix JD (1995) Isolation of a psaF-deficient mutant of Chlamydomonas reinhardtii: efficient interaction of plastocyanin with the photosystem I reaction center is mediated by the PsaF subunit. EMBO J 14:4976–4984

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garczarek L, Hess WR, Holtzendorff J, van der Staay GW, Partensky F (2000) Multiplication of antenna genes as a major adaptation to low light in a marine prokaryote. Proc Natl Acad Sci U S A 97:4098–4101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauska GA, McCarty RE, Berzborn RJ, Racker E (1971) Partial resolution of the enzymes catalyzing photophosphorylation. VII. The function of plastocyanin and its interaction with a specific antibody. J Biol Chem 246:3524–3531

    CAS  PubMed  Google Scholar 

  • Hervas M, Navarro JA, De La Rosa MA (2003) Electron transfer between membrane complexes and soluble proteins in photosynthesis. Acc Chem Res 36:798–805

    Article  CAS  PubMed  Google Scholar 

  • Hervas M, Diaz-Quintana A, Kerfeld CA, Krogmann DW, De la Rosa MA, Navarro JA (2005) Cyanobacterial Photosystem I lacks specificity in its interaction with cytochrome c(6) electron donors. Photosynth Res 83:329–333

    Article  CAS  PubMed  Google Scholar 

  • Hippler M, Reichert J, Sutter M, Zak E, Altschmied L, Schröer U, Herrmann RG, Haehnel W (1996) The plastocyanin binding domain of photosystem I. EMBO J 15:6374–6384

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hippler M, Drepper F, Haehnel W, Rochaix JD (1998) The N-terminal domain of PsaF: precise recognition site for binding and fast electron transfer from cytochrome c6 and plastocyanin to photosystem I of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 95:7339–7344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurt E, Hauska G (1981) A cytochrome f/b6 complex of five polypeptides with plastoquinol-plastocyanin-oxidoreductase activity from spinach chloroplasts. Eur J Biochem 117:591–595

    Article  CAS  PubMed  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917

    Article  CAS  PubMed  Google Scholar 

  • Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86–89

    Article  CAS  PubMed  Google Scholar 

  • Malakhov MP, Wada H, Los DA, Semenenko VE, Murata N (1994) A new type of cytochrome c from Synechocystis PCC6803. J Plant Physiol 144:259–264

    Article  CAS  Google Scholar 

  • Malakhov MP, Malakhova OA, Murata N (1999) Balanced regulation of expression of the gene for cytochrome cM and that of genes for plastocyanin and cytochrome c6 in Synechocystis. FEBS Lett 444:281–284

    Article  CAS  PubMed  Google Scholar 

  • Mann NH, Cook A, Millard A, Bailey S, Clokie M (2003) Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424:741

    Article  CAS  PubMed  Google Scholar 

  • Marcaida MJ, Schlarb-Ridley BG, Worrall JA, Wastl J, Evans TJ, Bendall DS, Luisi BF, Howe CJ (2006) Structure of cytochrome c6A, a novel dithio-cytochrome of Arabidopsis thaliana, and its reactivity with plastocyanin: implications for function. J Mol Biol 360:968–977

    Article  CAS  PubMed  Google Scholar 

  • Mazor Y, Greenberg I, Toporik H, Beja O, Nelson N (2012) The evolution of photosystem I in light of phage-encoded reaction centres. Philos Trans R Soc Lond B Biol Sci 367:3400–3405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazor Y, Nataf D, Toporik H, Nelson N (2014) Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803. Elife 3:e01496

    Article  PubMed Central  Google Scholar 

  • Molina-Heredia FP, Balme A, Hervás M, Navarro JA, De la Rosa MA (2002) A comparative structural and functional analysis of cytochrome cM cytochrome c6 and plastocyanin from the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 517:50–54

    Article  CAS  PubMed  Google Scholar 

  • Molina-Heredia FP, Wastl J, Navarro JA, Bendall DS, Hervás M, Howe CJ, De La Rosa MA (2003) Photosynthesis: a new function for an old cytochrome? Nature 424:33–34

    Article  CAS  PubMed  Google Scholar 

  • Molitor VR, Erber W, Peschek GA (1986) Increased levels of cytochrome oxidase and sodium-proton antiporter in the plasma membrane of Anacystis nidulans after growth in sodium-enriched media. FEBS Lett 204:251–256

    Article  CAS  Google Scholar 

  • Muller MG, Niklas J, Lubitz W, Holzwarth AR (2003) Ultrafast transient absorption studies on Photosystem I reaction centers from Chlamydomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in Photosystem I. Biophys J 85:3899–3922

    Article  PubMed  PubMed Central  Google Scholar 

  • Nelson N (2011) Photosystems and global effects of oxygenic photosynthesis. Biochim Biophys Acta 1807:856–863

    Article  CAS  PubMed  Google Scholar 

  • Nelson N, Neumann J (1972) Isolation of a cytochrome b 6 -f particle from chloroplasts. J Biol Chem 247:1817–1824

    CAS  PubMed  Google Scholar 

  • Partensky F, Garczarek L (2010) Prochlorococcus: advantages and limits of minimalism. Ann Rev Mar Sci 2:305–331

    Article  PubMed  Google Scholar 

  • Partensky F, Hess WR, Vaulot D (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63:106–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peschek GA, Obinger C, Paumann M (2004) The respiratory chain of blue-green algae (cyanobacteria). Physiol Plant 120:358–369

    Article  CAS  PubMed  Google Scholar 

  • Rieske JS, Zaugg WS, Hansen RE (1964) Studies on the electron transfer system. Lix. Distribution of iron and of the component giving an electron paramagnetic resonance signal at G = 1.90 in subfractions of complex 3. J Biol Chem 239:3023–3030

    CAS  PubMed  Google Scholar 

  • Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, …, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042–1047

    Google Scholar 

  • Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, …, Venter JC (2007) The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5:e77

    Google Scholar 

  • Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, …, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73:249–299

    Google Scholar 

  • Sharon I, Alperovitch A, Rohwer F, Haynes M, Glaser F, Atamna-Ismaeel N, Pinter RY, …, Beja O (2009) Photosystem I gene cassettes are present in marine virus genomes. Nature 461:258–262

    Google Scholar 

  • Sharon I, Battchikova N, Aro EM, Giglione C, Meinnel T, Glaser F, Pinter RY, …, Béjà O (2011) Comparative metagenomics of microbial traits within oceanic viral communities. ISME J 5:1178–1190

    Google Scholar 

  • Smith A, Witty M (2002) Heme, Chlorophyll, and Bilins: Methods and Protocols. Humana Press, Totowa

    Google Scholar 

  • Sommer F, Drepper F, Hippler M (2002) The luminal helix l of PsaB is essential for recognition of plastocyanin or cytochrome c6 and fast electron transfer to photosystem I in Chlamydomonas reinhardtii. J Biol Chem 277:6573–6581

    Article  CAS  PubMed  Google Scholar 

  • Sullivan MB, Waterbury JB, Chisholm SW (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424:1047–1051

    Article  CAS  PubMed  Google Scholar 

  • Sullivan MB, Lindell D, Lee JA, Thompson LR, Bielawski JP, Chisholm SW (2006) Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts. PLoS Biol 4, e234

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun J, Xu W, Hervás M, Navarro JA, Rosa MA, Chitnis PR (1999) Oxidizing side of the cyanobacterial photosystem I. Evidence for interaction between the electron donor proteins and a luminal surface helix of the PsaB subunit. J Biol Chem 274:19048–19054

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses – major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  PubMed  Google Scholar 

  • Szutka A (1966) Formation of pyrrolic compounds by ultra-violet irradiation of delta-aminolevulinic acid. Nature 212:401–402

    Article  CAS  PubMed  Google Scholar 

  • Weigel M, Varotto C, Pesaresi P, Finazzi G, Rappaport F, Salamini F, Leister D (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289

    Article  CAS  PubMed  Google Scholar 

  • Worrall JA, Schlarb-Ridley BG, Reda T, Marcaida MJ, Moorlen RJ, Wastl J, Hirst J, …, Howe CJ (2007) Modulation of heme redox potential in the cytochrome c6 family. J Am Chem Soc 129:9468–9475

    Google Scholar 

  • Wynn RM, Malkin R (1988) Interaction of plastocyanin with photosystem I: a chemical cross-linking study of the polypeptide that binds plastocyanin. Biochemistry 27:5863–5869

    Article  CAS  PubMed  Google Scholar 

  • Zatwarnicki P, Barciszewski J, Krzywda S, Jaskolski M, Kolesinski P, Szczepaniak A (2013) Cytochrome c(6B) of Synechococcus sp. WH 8102 – crystal structure and basic properties of novel c(6)-like family representative. Biochem Biophys Res Commun 443:1131–1135

    Article  PubMed  Google Scholar 

  • Zeidner G, Bielawski JP, Shmoish M, Scanlan DJ, Sabehi G, Béjà O (2005) Potential photosynthesis gene recombination between Prochlorococcus and Synechococcus via viral intermediates. Environ Microbiol 7:1505–1513

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathan Nelson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Mazor, Y., Nelson, N. (2016). Higher Plant and Cyanobacterial Photosystem I: Connected Cytochrome Pathways. In: Cramer, W., Kallas, T. (eds) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Advances in Photosynthesis and Respiration, vol 41. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7481-9_7

Download citation

Publish with us

Policies and ethics