Skip to main content
SpringerLink
Log in

Hypothesis: the peroxydicarbonic acid cycle in photosynthetic oxygen evolution

  • Original Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Peroxydicarbonic acid (Podca), a proposed intermediate in photosynthetic oxygen evolution, was synthesized electrochemically. Consistent with literature descriptions of this compound, it was shown to be a highly reactive molecule, spontaneously hydrolyzed to H2O2, as well as susceptible to oxidative and reductive decomposition. In the presence of Mn2+ or Co2+, Podca was quickly broken down with release of O2. The liberation of O2, however, was partially suppressed at high O2 concentrations. In the presence of Ca-washed photosystem II-enriched membranes lacking extrinsic proteins, Podca was decomposed with the release of O2, but only under conditions favoring photosynthetic electron flow (light plus a Hill oxidant). A model is proposed that details how peroxydicarbonic acid could act as an oxygen-evolving intermediate. The hypothesis is consistent with the well-established Kok model and with recent findings related to the chemistry of oxygen evolution.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Scheme 1
Fig. 2
Fig. 3
Fig. 4
Scheme 2
Fig. 5
Fig. 6
Fig. 7
Scheme 3
Scheme 4
Scheme 5

Similar content being viewed by others

Abbreviations

CA:

Carbonic anhydrase

Podca:

Peroxydicarbonic acid

References

  • Ananyev G, Wydrzynski T, Renger G, Klimov VV (1992) Transient peroxide formation by the manganese-containing, redox-active donor side of photosystem II upon inhibition of O2 evolution with lauroylcholine chloride. Biochim Biophys Acta 1100:303–311

    Google Scholar 

  • Bentley R (1978) Ogston and the development of prochirality theory. Nature 276:673–676

    Article  CAS  Google Scholar 

  • Bentley R (2003) Diasterioisomerism, contact points, and chiral selectivity: a four-site saga. Arch Biochim Biophys 414:1–12

    Article  CAS  Google Scholar 

  • Carpentier R, Fuerst EP, Nakatani HY, Arntzen CJ (1985) A second site for herbicide action in photosystem II. Biochim Biophys Acta 808:293–299

    Article  CAS  Google Scholar 

  • Clausen J, Jünge W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430:480–483

    Article  PubMed  CAS  Google Scholar 

  • Constam EJ, von Hansen A (1896–1897) Electrolytische Darstellung einer neuen Klasse oxydierender Substanzen. Zeitsch Elekt 3:137–144

  • Elbs K, Schönherr O (1894) Studien über die Bildung von Überschwefelsaüre. Zeitsch Elekt 1:417–420

    Google Scholar 

  • Hashimoto A, Yamamoto Y, Theg SM (1996) Unassembled subunits of the photosynthetic oxygen-evolving complex present in the thylakoid lumen are long-lived and assembly-competent. FEBS Lett 391:29–34

    Article  PubMed  CAS  Google Scholar 

  • Hendry G, Wydrzynski T (2002) The two substrate-water molecules are already bound to the oxygen-evolving complex in the S2 state of photosystem II. Biochemistry 41:13328–13334

    Article  PubMed  CAS  Google Scholar 

  • Hillier W, McConnell I, Badger MR, Boussac A, Klimov VV, Dismukes GC, Wydrzynski T (2006) Quantitative assessment of intrinsic carbonic anhydrase activity and the capacity for bicarbonate oxidation in photosystem II. Biochemistry 45:2094–2101

    Google Scholar 

  • Hillier W, Messinger J (2005) Mechanisms of photosynthetic oxygen production. In: Wydrzynski TJ, Satoh K, Freeman JA (eds) Photosystem II: the light-driven water plastoquinone oxidoreductase. Springer, Dordrecht, pp 567–608

    Google Scholar 

  • Hillier W, Wydrzynski T (1993) Increases in peroxide formation by the photosystem II oxygen evolving reactions upon removal of the extrinsic 16, 22 and 33 kDa proteins are reversed by CaCl2 addition. Photosynth Res 38:417–423

    Article  CAS  Google Scholar 

  • Joliot P, Barbieri G, Chabaud R (1969) Un nouveau modele des centres photochimiques du systeme II. Photochem Photobiol 10:309–329

    CAS  Google Scholar 

  • Khomutov NE, Filatova LS (1974) Izlichenije kinetiki Gomogenno-kataliticheskogo razlozhenija peroksokarbonata kalija. (Transcribed into Roman alphabet) Trudy Instituta Moskovskii Khïmiko-technologicheskii institut im D. I. Mendeleeva 81:21–23

    Google Scholar 

  • Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution. Photochem Photobiol 11:437–475

    Google Scholar 

  • Kreutz W (1974) Considerations on water-splitting in photosynthesis. In: Colbow K (ed) On the physics of biological membranes. Department of Physics, Simon Fraser University, Vancouver, pp 419–429

    Google Scholar 

  • Kuwabara T, Murata N (1983) Quantitative analysis of the inactivation of photosynthetic oxygen evolution and the release of peptides and manganese in photosystem II particles of spinach chloroplasts. Plant Cell Physiol 24:741–747

    CAS  Google Scholar 

  • Kuwabara T, Miyao M, Murata T, Murata N (1985) The function of 33-kDa protein in the photosynthetic oxygen-evolution system studied by reconstitution experiments. Biochim Biophys Acta 806:283–289

    Article  CAS  Google Scholar 

  • Liochev SI, Fridovich I (2004) Carbon dioxide mediates Mn(II)-catalyzed decomposition of hydrogen peroxide and peroxidation reactions. Proc Natl Acad Sci USA 101(34):12482–12490

    Article  Google Scholar 

  • Lu Y-K, Stemler AJ (2002) Extrinsic photosystem II carbonic anhydrase in maize mesophyll chloroplasts. Plant Physiol 128:643–649

    Google Scholar 

  • Lu Y-K, Theg SM, Stemler AJ (2005) Carbonic anhydrase activity of the photosystem II OEC33 protein from pea. Plant Cell Physiol 46(12):1944–1953

    Google Scholar 

  • Metzner H (1978) Oxygen evolution as energetic problem. In: Metzner H (ed) Photosynthetic oxygen evolution. Academic Press, London, pp 59–76

    Google Scholar 

  • Moskvin OV, Shutova TV, Khristin MS, Ignatova LK, Villarejo A, Samuelson G, Klimov VV, Ivanov BN (2004) Carbonic anhydrase activities in pea thylakoids. Photosynth Res 79:93–100

    Article  PubMed  CAS  Google Scholar 

  • Ogston AG (1948) Interpretation of experiments on metabolic processes using isotopic tracer elements. Nature 162(2):963

    Google Scholar 

  • Partington JR, Fathallah AH (1950) Inorganic per-acids. Part II. The alkali percarbonates. J Chem Soc Lond 1934–1943

  • Renger G (1978) Theoretical studies about the functional and structural organization of the photosynthetic oxygen evolution. In: Metzner H (ed) Photosynthetic oxygen evolution. Academic Press, London, pp 229–248

    Google Scholar 

  • Riesenfeld EH, Mau W (1911) Isomere percarbonate. Ber d Deut Chem Gesellschaft 3595–3605

  • Riesenfeld EH, Reinhold R (1910) Die Existenz echter Percarbonate und ihre Unterscheidung von Carbonaten mit Krystall-Wasserstoffsuperoxyd. Ber d Deut Chem Gesellshaft 42:4377–4383

  • Stadtman ER, Bertlett BS, Chock PB (1990) Manganese-dependent disproportionation of hydrogen peroxide in bicarbonate buffer. Proc Natl Acad Sci USA 87:384–388

    Article  PubMed  CAS  Google Scholar 

  • Stemler A (1977) The binding of bicarbonate ions to washed chloroplast membranes. Biochim Biophys Acta 460:511–522

    Article  PubMed  CAS  Google Scholar 

  • Stemler AJ (2002) The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg. Photosynth Res 73:177–183

    Article  PubMed  CAS  Google Scholar 

  • Stemler A, Murphy J (1984) Inhibition of HCO −3 binding to photosystem II by atrazine at a low-affinity herbicide binding site. Plant Physiol 76:179–182

    Google Scholar 

  • Tanatar S (1899) Percarbonate. Ber d Deut Chem Gesellschaft 32:1544–1546

  • Velthuys B, Kok B (1978) Photosynthetic oxygen evolution from hydrogen peroxide. Biochim Biophys Acta 502:211–221

    Article  PubMed  CAS  Google Scholar 

  • Volkov AG (1989) Oxygen evolution in the course of photosynthesis: molecular mechanisms. Bioelectrochem Bioenerget 21:3–24

    Article  CAS  Google Scholar 

  • Wolffenstein R, Peltner E (1908) Zur Kenntnis überkohlensaurer Salze. Ber d Deut Chem Gesellschaft 41:280–297

  • Xu Q, Bricker TM (1992) Structural organization of proteins on the oxidizing side of photosystem II: Two molecules of the 33-kDa manganese-stabilizing protein per reaction center. J Bio Chem 267:25816–25821

    CAS  Google Scholar 

  • Yachandra VK (2005) The catalytic manganese cluster: organization of the metal ions. In: Wydrzynski TJ, Satoh K, Freeman JA (eds) Photosystem II, the light-driven water-plastoquinone oxidoreductase. Springer, Dordrecht, pp 235–260

    Google Scholar 

Download references

Author information

Author notes

  1. Yih-Kuang Lu

    Present address: Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ, 85287, USA

Authors and Affiliations

  1. Section of Plant Biology, University of California, Davis, CA, 95616, USA

    Paul A. Castelfranco & Alan J. Stemler

Authors
  1. Paul A. Castelfranco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yih-Kuang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alan J. Stemler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alan J. Stemler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Castelfranco, P.A., Lu, YK. & Stemler, A.J. Hypothesis: the peroxydicarbonic acid cycle in photosynthetic oxygen evolution. Photosynth Res 94, 235–246 (2007). https://doi.org/10.1007/s11120-007-9134-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9134-8

Keywords

Search

Navigation