Skip to main content
SpringerLink
Log in

The Origin and Evolution of Photosynthetic Oxygen Production

  • Chapter
Photosystem II

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 22))

Summary

This chapter reviews some of the evidence and the postulated proposals for how oxygenic photosynthesis first emerged as a distinct form of photoautotrophic metabolism using water as an electron donor. This form of photosynthesis is the most successful photoautotrophic metabolism in the contemporary biosphere and is found in all higher plants, green and red algae and both cyano- and oxyphoto-bacteria. We summarize the timetable for emergence and the biogeochemical consequences of oxygenic photosynthesis. Particular attention is paid to evolution of the inorganic core of the enzyme that catalyzes water oxidation, chemical speciation of the inorganic cofactors and possible alterative substrates. We discuss possible mineral remnants of early oxygenic photosynthesis and the emerging role of bicarbonate in assembly of the inorganic core and as an hypothesized evolutionary cofactor.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 509.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 649.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrahamsson MLA, Baudin HB, Tran A, Philouze C, Berg KE, Raymond-Johansson MK, Sun LC, Akermark B, Styring S and Hammarstrom L (2002) Ruthenium-manganese complexes for artificial photosynthesis: Factors controlling intramolecular electron transfer and excited-state quenching reactions. Inorg Chem 41: 1534–1544

    Article  CAS  PubMed  Google Scholar 

  • Ananyev GM and Dismukes GC (2005) How fast can Photosystem II split water? Kinetic performance at high and low frequencies. Photosynth Res, in press

    Google Scholar 

  • Ananyev GM, Murphy A, Abe Y and Dismukes GC (1999) Remarkable affinity and selectivity for Cs+ and uranyl (UO22+) binding to the manganese site of the apo-water oxidation complex of Photosystem II. Biochemistry 38: 7200–7209

    Article  CAS  PubMed  Google Scholar 

  • Ananyev GM, Zaltsman L, Vasko C and Dismukes GC (2001) The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim Biophys Acta 1503: 52–68

    CAS  PubMed  Google Scholar 

  • Baranov SV, Ananyev GM, Klimov VV and Dismukes GC (2000) Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted Photosystem II: A proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis. Biochemistry 39: 6060–6065

    Article  CAS  PubMed  Google Scholar 

  • Baranov S, Tyryshkin A, Katz D, Ananyev G, Klimov V and Dismukes G (2004) Bicarbonate is a native cofactor for assembly of the manganese cluster of the photosynthetic water oxidizing complex: II. Kinetics of reconstitution of O2 evolution by photoactivation. Biochemistry 43: 2070–2079

    Article  CAS  PubMed  Google Scholar 

  • Blankenship RE (2002) Molecularmechanisms of photosynthesis. Oxford, Blackwell Science

    Google Scholar 

  • Blankenship RE and Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23: 94–97

    Article  CAS  PubMed  Google Scholar 

  • Boussac A and Rutherford AW (1988) The nature of the inhibition of the oxygen evolving enzyme of PS II which is induced by NaCl washing and reversed by the addition of Ca2+ or Sr2+. Biochemistry 27: 3476–3483

    Article  CAS  Google Scholar 

  • Bruhland K (1983). Trace elements in seawater. In: Riley JP and Chester R (eds) Chemical Oceanography, pp 147–220. Academic Press, London

    Google Scholar 

  • Brune D (1995) Sulfur compounds as photosynthetic electron donors. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 847–870, Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Carrell TG, Tyryshkin A and Dismukes GC (2002) An evaluation of structural model for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7: 2–22

    Article  CAS  PubMed  Google Scholar 

  • Catling DC, Zahlne KJ and McKay CP (2001) Biogenic methane, hydrogen escape and the irreversible oxidation of early Earth. Science 293(5531): 839–842

    Article  CAS  PubMed  Google Scholar 

  • Cloud PE (1972) Atmospheric and hydrospheric evolution on the primitive Earth. Science 160: 729–736

    Google Scholar 

  • Cohen Y, Jorgensen, BB, Revsbech, NP and Poplawski R (1986) Adaptation to hydrogen-sulfide of oxygenic and anoxygenic photosynthesis among cyanobacteria. Appl Environ Microbiol 51:398–407

    CAS  PubMed  Google Scholar 

  • Dasgupta J, van Willigen RT and Dismukes GC (2004) Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: Functional roles for calcium and bicarbonate. Phys Chem Chem Phys 6: 4793–4802

    CAS  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102: 269–352

    CAS  PubMed  Google Scholar 

  • Debus RJ (2000) The polypeptides of Photosystem II and their influence on manganotyrosyl-based oxygen evolution. In: Sigel A and Sigel H (eds) Metal Ions in Biological Systems: Manganese and Its Role in Biological Processes, pp 657–711. Marcel Dekker Inc, New York

    Google Scholar 

  • Debus RJ (2001) Amino acidresidues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of PS II. Biochim Biophys Acta 1503: 164–186

    CAS  PubMed  Google Scholar 

  • Des Marais DJ (2000) When did photosynthesis emerge on Earth? Science 289: 1703–1704

    PubMed  Google Scholar 

  • Diner BA (1998) Application of spectroscopic techniques to the study of PS II mutations engineered in Synechocystis and Chlamydomonas. Meth Enzymol 297: 337–360

    CAS  Google Scholar 

  • Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of Photosystem II. Proton-coupled electron transport of the redoxactive tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503:147–163

    CAS  PubMed  Google Scholar 

  • Diner BA and Rappaport F (2002) Structure, dynamics and energetics of the primary photochemistry of PS II on oxygenic photosynthesis. Annu Rev Plant Biol: 551–580

    Google Scholar 

  • Dismukes GC (1988) The spectroscopically derived structure of the manganese site for photosynthetic water oxidization and a proposal for the protein-binding sites for calcium and manganese. Chemica Scripta 28A: 99–104

    Google Scholar 

  • Dismukes GC, Ruettinger W, Boelrijk AEM and Ho D (1998) Structure of the mn4cal core of the PS II water oxidizing complex and the Mn4O4-cubane/Mn4O2-butterfly model complexes. In: Garab G (ed) Photosynthesis: Mechanisms and Effects, Vol II, pp 1259–1264. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, Dasgupta J and Tyryshkin A (2001) The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis. Proc Nat Acad Sci USA 98: 2170–2175

    Article  CAS  PubMed  Google Scholar 

  • Farquhar J, Bao HN and Thiemans M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289: 756

    Article  CAS  PubMed  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Grotzinger JP and Kasting JF (1993) New constraints onprecam-brian ocean composition. J Geol 101(2): 235–243

    CAS  PubMed  Google Scholar 

  • Hedges S, Chen H, Kumar H, Wang D Y-C, Thomson AS and Watanabe H (2001) A genomic timescale for the origin of eukaryotes. BMC Evol Biol 1: 4

    Article  CAS  PubMed  Google Scholar 

  • Holland HD (1984) Chemical Evolution of the Atmosphere and Oceans. Princeton University Press, Princeton

    Google Scholar 

  • Holland H and Rye R (1998) Paleo-reconstruction of early O2 evolution. Amer J Science 298: 621–672

    Google Scholar 

  • Hu QM, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M and Itoh S (1998) A Photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci USA 95: 13319–13323

    CAS  PubMed  Google Scholar 

  • Itoh S, Iwaki M, Noguti T, Kawamori A and Mino H (2001) In: PS2001 Proceedings: 12th International Congress on Photosynthesis, S6-028. CSIRO Publishing, Melbourne (CD-ROM)

    Google Scholar 

  • Kálmán L, LoBrutto, Allen JP and Williams JC (1999) Modified reaction centers oxidize tyrosine in reactions that mirror PS II. Nature 402: 696–699

    Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7-Ã… resolution. Proc Nat Acad Sci USA 100: 98–103

    Article  CAS  PubMed  Google Scholar 

  • Kasting J (1993) Earth’s early atmosphere. Science 259: 920–926

    CAS  PubMed  Google Scholar 

  • Kasting JF and Seifert JL (2002) Life and the evolution of Earth’s atmosphere. Science 296: 1066–1068

    Article  CAS  PubMed  Google Scholar 

  • Klimov VV and Baranov SV (2001) Bicarbonate requirement for the water-oxidizing complex of Photosystem II. Biochim Biophys Acta 1503: 187–196

    CAS  PubMed  Google Scholar 

  • Kozlov YN, Kazakova AA and Klimov VV (1997) Changes in the redox-potential and catalase activity of Mn2+ ions during formation of Mn-bicarbonate complexes. Biologicheskie Membrany (Russian) 14: 93–97

    CAS  Google Scholar 

  • Kozlov YN, Zharmukhamedov SK, Tikhonov KG, Dasgupta J, Kazakova AA, Dismukes GC and Klimov VV (2004) Oxidation potentials and electron donation to Photosystem II of manganese complexes containing bicarbonate and carboxylate ligands. Phys Chem Chem Phys 6: 4905–4911

    Article  CAS  Google Scholar 

  • Lasaga A and Ohmoto H (2002) The oxygen geochemical cycle: Dynamics and stability. Geochim Cosmochim Acta 66:361–381

    Article  CAS  Google Scholar 

  • Mimuro M, Akimoto S, Yamazaki I, Miyashita H and Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga Acaryochloris marina: Studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412: 37–46

    CAS  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M and Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383: 402

    Article  CAS  Google Scholar 

  • Morse JW and Mackenzie FT (1998) Hadean ocean carbonate geochemistry. Aquatic Geochem 4: 301–319

    CAS  Google Scholar 

  • Ohmoto H (1997) When did the Earth’s atmosphere become oxic? Geochem News 97: 26–27

    Google Scholar 

  • Olson JM (1970) The evolution of photosynthesis. Science 168: 438–446

    CAS  PubMed  Google Scholar 

  • Olson JM (2001) ‘Evolution of photosynthesis’ (1970) re-examined thirty years later. Photosynth Res 68: 95–112

    Article  CAS  PubMed  Google Scholar 

  • Olson JM and Blankenship RE (2004) Thinking about the evolution of photosynthesis. Photosynth Res 80: 373–386

    CAS  PubMed  Google Scholar 

  • Raven JA, Evans MCW and Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60: 111–149

    Article  CAS  Google Scholar 

  • Robblee JH, Cinco RM and Yachandra VK (2001) X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503: 7–23

    CAS  PubMed  Google Scholar 

  • Ruettinger W, Yagi M, Wolf K, Bernasek S and Dismukes GC (2000) O2 evolution from the manganese-oxo cubane core [Mn4O4]6+: A molecular mimic of the photosynthetic water oxidation enzyme? J Am Chem Soc 122: 10353–10357

    Article  CAS  Google Scholar 

  • Russell MJ and Hall AJ (2002) From geochemistry to biochemistry: Chemiosmotic coupling and transition element clusters in the onset of life and photosynthesis. Geochem News 113: 6–12

    Google Scholar 

  • Russell MJ, Hall AJ and Mellersh AR (2003) On the dissipation of thermal and chemical energies on the early Earth: The onsets of hydrothermal convection, chemiosmosis, genetically regulated metabolism and oxygenie photosynthesis. In: Ikan R (ed) Natural and Laboratory-Simulated Thermal Geochemical Processes. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Sauer K and Yachandra VK (2002) A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean. Proc Nat Acad Sci USA 99: 8631–8636

    Article  CAS  PubMed  Google Scholar 

  • Semin BK, Ghirardi ML and Seibert M (2002) Blocking of electron donation my Mn(II) to Yz following incubation of Mn-depleted PS II membranes with Fe(II) in the light. Biochemistry 41: 5854–5864

    Article  CAS  PubMed  Google Scholar 

  • Smith RM and Martell AE (1976) Critical Stability Constants. Plenum, New York

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sugisaki R, Horiuchi Y, Sugitani K and Adachi M (1995) Acid character of archean ocean waters revealed by 3.3-Ga-old ferruginous chart compositions, Western-Australia. Proc Japan Acad: B-Phys Biol Sci 71: 170–174

    Google Scholar 

  • Summons RE, Jahnke LL, Hope JM and Logan GA (1999) 2-methylhopanoids as biomarkers for cyanobacteria oxygenic photosynthesis. Nature 400: 554–557

    Article  CAS  PubMed  Google Scholar 

  • Svensson B, Etchebest C, Tuffery P, Van Kan P, Smith J and Styring S (1996) A model for the Photosystem II reaction center core including the structure of the primary donor P680. Biochemistry 35: 14486–14502

    Article  CAS  PubMed  Google Scholar 

  • Sychev AY and Isac VG (1993) The catalase, peroxidase, and oxidase properties of the coordination compounds of manganese. Russ Chem Rev 62: 279–290

    Article  Google Scholar 

  • Towe KM (1994) Earth’s early atmosphere: Constraints and opportunities for early evolution. In: Early Life on Earth, Nobel Symposium No 84, Columbia University Press, New York

    Google Scholar 

  • Vrettos JS, Stone DA and Brudvig GW (2001) Quantifying the ion selectivity of the Ca2+ site in Photosystem II: Evidence for direct involvement of Ca2+ in O2 formation. Biochemistry 40:7937–7945

    Article  CAS  PubMed  Google Scholar 

  • Walker JCG (1985) Carbon dioxide on the early Earth. Orig Life Evol Biosph 16: 117–127

    Article  CAS  PubMed  Google Scholar 

  • Xiong J, Subramanium S and Govindjee (1998) A knowledge-based three dimensional model of the Photosystem II reaction center of Chlamydomonas reinhardtii. Photosynth Res 56: 229–254

    Article  CAS  Google Scholar 

  • Xiong J, Fisher WM, Inoue K, Narakhara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730

    Article  CAS  PubMed  Google Scholar 

  • Yagi M, Wolf KV, Baesjou PJ, Bernasek SL and Dismukes GC (2001) Selective photoproduction of O2 from the Mn4O4 cubane core: A structural and functional model for the photosynthetic water oxidizing complex. Angew Chem Int Ed 40: 2925–2928

    Article  CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W and Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Ã… resolution. Nature 409: 739–743

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and Princeton Environmental Institute, Princeton University, Princeton, NJ, 08544, USA

    G. Charles Dismukes

  2. Department of Chemistry and Biochemistry, Arizona State University, Tempe, AZ, 85287-1604, USA

    Robert E. Blankenship

Authors
  1. G. Charles Dismukes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert E. Blankenship
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. The Australian National University, Canberra, Australia

    Thomas J. Wydrzynski

  2. Okayama University, Okayama, Japan

    Kimiyuki Satoh

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Springer

About this chapter

Cite this chapter

Dismukes, G.C., Blankenship, R.E. (2005). The Origin and Evolution of Photosynthetic Oxygen Production. In: Wydrzynski, T.J., Satoh, K., Freeman, J.A. (eds) Photosystem II. Advances in Photosynthesis and Respiration, vol 22. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4254-X_31

Download citation

Publish with us

Policies and ethics

Search

Navigation