Skip to main content

On the Nature of the Functional S-States in the Oxygen Evolving Centre of Photosystem II—What Computational Chemistry Reveals About the Water Splitting Mechanism

  • Chapter
  • First Online:
Photosynthesis: Molecular Approaches to Solar Energy Conversion

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 47))

  • 1299 Accesses

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 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
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

References

  • Åhrling KA, Pace RJ (2005) The catalytic manganese cluster: implications from spectroscopy. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: The Light-Driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht, pp 285–305

    Google Scholar 

  • Ananyev G, Wydrzynski T, Renger G, Klimov V (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 

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

    Google Scholar 

  • Cox N, Messinger J (2013) Reflections on substrate water and dioxygen formation. Biochim Biophys Acta 1827:1020–1030

    Google Scholar 

  • Dau H, Limberg C, Reier T, Risch M, Roggan S, Strasser P (2010) The mechanism of water oxidation: from electrolysis via homogeneous to biological catalysis. Chem Cat Chem 2:724–761

    Google Scholar 

  • Davis KM, Sullivan BT, Palenik MC, Yan L, Purohit V, Robison G, Kosheleva I, …, Pushkar Y (2018) Rapid evolution of the photosystem II electronic structure during water splitting. Phys Rev X 8:1252–1257

    Google Scholar 

  • de Wijn R, Schrama T, van Gorkom HJ (2001) Secondary stabilization reactions and proton-coupled electron transport in photosystem II investigated by electroluminescence and fluorescence spectroscopy. Biochemistry 40:5821–5834

    Google Scholar 

  • Gatt P, Stranger R, Pace RJ (2011) Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II – a review. J Photochem Photobiol B 104:80–93

    Google Scholar 

  • Gatt P, Petrie S, Stranger R, Pace RJ (2012) Rationalizing the 1.9 Å crystal structure of photosystem II-a remarkable Jahn-Teller balancing act induced by a single proton transfer. Angew Chem 124:12191–12194

    Google Scholar 

  • Glöckner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J (2013) Structural changes of the oxygen-evolving complex in photosystem II during the catalytic cycle. J Biol Chem 288:22607–22620

    Google Scholar 

  • Groves JT, Lee J, Marla SS (1997) Detection and characterization of an oxomanganese(V) porphyrin complex by rapid-mixing stopped-flow spectrophotometry. J Am Chem Soc 119:6269–6273

    Google Scholar 

  • Grundmeier A, Dau H (2012) Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim Biophys Acta 1817:88–105

    Google Scholar 

  • Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, …, Dau H (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44:1894–1908

    Google Scholar 

  • Hendry G, Wydrzynski T (2003) 18O isotope exchange measurements reveal that calcium is involved in the binding of one substrate-water molecule to the oxygen-evolving complex in photosystem II. Biochemistry 42:6209–6217

    Google Scholar 

  • Hillier W, Wydrzynski T (2001) Oxygen ligand exchange at metal sites - implications for the O2 evolving mechanism of photosystem II. Biochim Biophys Acta 1503:197–209

    Google Scholar 

  • Hillier W, Wydrzynski T (2004) Substrate water interactions within the photosystem II oxygen evolving complex. Phys Chem Chem Phys 6:4882

    Google Scholar 

  • Hillier W, Wydrzynski T (2008) 18O-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252:306–317

    Google Scholar 

  • Kern J, Chatterjee R, Young ID, Fuller FD, Lassalle L, Ibrahim M, Gul S, …, Yachandra VK (2018) Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature 563:421–425

    Google Scholar 

  • Klimov VV, Allakhverdiev SI, Shuvalov VA, Krasnovsky AA (1982) Effect of extraction and re-addition of manganese on light reactions of photosystem-II preparations. FEBS Lett 148:307–312

    Google Scholar 

  • Klimov VV, Shafiev MA, Allakhverdiev SI (1986) Photobiochem. Photo-Dermatology 12:61–65

    Google Scholar 

  • Klimov VV, Shafiev MA, Allakhverdiev SI (1990) Photoinactivation of the reactivation capacity of photosystem II in pea subchloroplast particles after a complete removal of manganese. Photosynth Res 23:59–65

    Google Scholar 

  • Klimov VV, Ananyev GM, Zastrizhnaya OM (1992) In: Murata N (ed) Research in Photosynthesis, vol 2. Kluwer, Dordrecht, pp 441–444

    Google Scholar 

  • Klimov V, Ananyev G, Zastryzhnaya O, Wydrzynski T, Renger G (1993) Photoproduction of hydrogen peroxide in photosystem II membrane fragments: a comparison of four signals. Photosynth Res 38:409–416

    Google Scholar 

  • Koua FHM, Umena Y, Kawakami K, Shen J-R (2013) Structure of Sr-substituted photosystem II at 2.1 Å resolution and its implications in the mechanism of water oxidation. Proc Natl Acad Sci U S A 110:3889–3894

    Google Scholar 

  • Krewald V, Retegan M, Cox N, Messinger J, Lubitz W, DeBeer S, Neese F, Pantazis DA (2015) Metal oxidation states in biological water splitting. Chem Sci 6:1676–1695

    Google Scholar 

  • Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA, Rendek KN, Hunter MS, …, Fromme P (2014) Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–265

    Google Scholar 

  • Kuzek D, Pace RJ (2001) Probing the Mn oxidation states in the OEC. Insights from spectroscopic, computational and kinetic data. Biochim Biophys Acta 1503:123–137

    Article  CAS  Google Scholar 

  • Li X, Siegbahn PEM (2015) Alternative mechanisms for O2 release and O–O bond formation in the oxygen evolving complex of photosystem II. Phys Chem Chem Phys 17:12168–12174

    Google Scholar 

  • Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, …, Yachandra VK (2001) Absence of Mn-centered oxidation in the S2 → S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123:7804–7820

    Google Scholar 

  • Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL (1992) Nature of biological electron transfer. Nature 355:796–802

    Google Scholar 

  • Nilsson H, Rappaport F, Boussac A, Messinger J (2014) Substrate–water exchange in photosystem II is arrested before dioxygen formation. Nat Commun 5:261–265

    Google Scholar 

  • Pace RJ, Åhrling KA (2004) Water oxidation in PSII-H atom abstraction revisited. Biochim Biophys Acta 1655:172–178

    Google Scholar 

  • Pace RJ, Jin L, Stranger R (2012) What spectroscopy reveals concerning the Mn oxidation levels in the oxygen evolving complex of photosystem II: X-ray to near infra-red. Dalton Trans 41:11145–11160

    Google Scholar 

  • Pantazis DA, Ames W, Cox N, Lubitz W, Neese F (2012) Two interconvertible structures that explain the spectroscopic properties of the oxygen-evolving complex of photosystem II in the S2 state. Angew Chem Int Ed 51:9935–9940

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2010a) Location of potential substrate water binding sites in the water oxidizing complex of photosystem II. Angew Chem Int Ed 49:4233–4236

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2010b) Hydration preferences for Mn4Ca cluster models of photosystem II: location of potential substrate-water binding sites. Chem Eur J 16:14026–14042

    Google Scholar 

  • Petrie S, Pace RJ, Stranger R (2015a) Resolving the differences between the 1.9Å and 1.95Å crystal structures of photosystem II: a single proton relocation defines two tautomeric forms of the water-oxidizing complex. Angew Chem Int Ed 54:7120–7124

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2015b) Rationalising the geometric variation between the A and B monomers in the 1.9Å crystal structure of photosystem II. Chem Eur J 21:6780–6792

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2017a) Rationalizing the 2.25Å resolution crystal structure of the water oxidising complex of photosystem II in the S3 state. Chem Phys Chem 18:2924–2931

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2017b) What Mn Kβ spectroscopy reveals concerning the oxidation states of the Mn cluster in photosystem II. Phys Chem Chem Phys 19:27682–27693

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2018) Explaining the different geometries of the water oxidising complex in the nominal S3 state crystal structures of photosystem II at 2.25Å and 2.35Å. Chem Phys Chem 19:3296–3309

    Google Scholar 

  • Pizarro SA, Glatzel P, Visser H, Robblee JH, Christou G, Bergmann U, Yachandra VK (2004) Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to photosystem II: Mn K-edge X-ray absorption and Kβ X-ray emission spectroscopy studies. Phys Chem Chem Phys 6:4864

    Google Scholar 

  • Pollock CJ, Delgado-Jaime MU, Atanasov M, Neese F, DeBeer S (2014) Kβ mainline X-ray emission spectroscopy as an experimental probe of metal-ligand covalency. J Am Chem Soc 136:9453–9463

    Google Scholar 

  • Pushkar Y, Yano J, Glatzel P, Messinger J, Lewis A, Sauer K, Bergmann U, Yachandra V (2006) Structure and orientation of the Mn4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy. J Biol Chem 282:7198–7208

    Google Scholar 

  • Rappaport F, Lavergne J (2001) Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim Biophys Acta 1503:246–259

    Google Scholar 

  • Rappaport F, Blanchard-Desce M, Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184:178–192

    Google Scholar 

  • Razeghifard MR, Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids and PSII membranes: a kinetic intermediate in the S3 to S0 transition. Biochemistry 38:1252–1257

    Google Scholar 

  • Wydrzynski TJ, Satoh K (eds) (2005) Photosystem II: The Light-driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht

    Google Scholar 

  • Sauer K, Yano J, Yachandra V (2008) X-ray spectroscopy of the photosynthetic oxygen-evolving complex. Coord Chem Rev 252:318–335

    Google Scholar 

  • Siegbahn PEM (2009) Structures and energetics for O2 formation in photosystem II. Acc Chem Res 42:1871–1880

    Google Scholar 

  • Siegbahn PEM (2013) Substrate water exchange for the oxygen evolving complex in PSII in the S1, S2, and S3 states. J Am Chem Soc 135:9442–9449

    Google Scholar 

  • Sproviero EM, Gascón JA, McEvoy JP, Brudvig GW, Batista VS (2008) Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. J Am Chem Soc 130:3428–3442

    Google Scholar 

  • Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, …, Shen J-R (2015) Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103

    Google Scholar 

  • Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, Nakane T, Yamashita K, …, Shen J-R (2017) Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543:131–135

    Google Scholar 

  • Taguchi M, Uozumi T, Kotani A (1997) Theory of X-ray photoemission and X-ray emission spectra in Mn compounds. J Phys Soc Jpn 66:247–256

    Google Scholar 

  • Terrett R, Petrie S, Stranger R, Pace RJ (2016) What computational chemistry and magnetic resonance reveal concerning the oxygen evolving centre in photosystem II. J Inorg Biochem 162:178–189

    Google Scholar 

  • Ugur I, Rutherford AW, Kaila VRI (2016) Redox-coupled substrate water reorganization in the active site of photosystem II—the role of calcium in substrate water delivery. Biochim Biophys Acta 1857:740–748

    Google Scholar 

  • Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60

    Google Scholar 

  • Vinyard DJ, Ananyev GM, Dismukes GC (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606

    Google Scholar 

  • Vinyard DJ, Khan S, Brudvig GW (2015) Photosynthetic water oxidation: binding and activation of substrate waters for O-O bond formation. Faraday Discuss 185:37–50

    Google Scholar 

  • Visser H, Anxolabéheìre-Mallart E, Bergmann U (2001) Mn K-edge XANES and Kβ XES studies of two Mn-oxo binuclear complexes: investigation of three different oxidation states relevant to the oxygen-evolving complex of photosystem II. J Am Chem Soc 123:7031–7039

    Google Scholar 

  • Wang J, Askerka M, Brudvig GW, Batista VS (2017) Crystallographic data support the carousel mechanism of water supply to the oxygen-evolving complex of photosystem II. ACS Energy Lett 2:2299–2306

    Google Scholar 

  • Wydrzynski T, Ångström J, Vänngård T (1989) H2O2 formation by photosystem II. Biochim Biophys Acta 973:23–28

    Google Scholar 

  • Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96:2927–2950

    Google Scholar 

  • Yamaguchi K, Isobe H, Yamanaka S, Saito T, Kanda K, Shoji M, Umena Y, …, Okumura M (2012) Full geometry optimizations of the mixed-valence CaMn4O4X(H2O)4 (X=OH or O) cluster in OEC of PS II: degree of symmetry breaking of the labile Mn-X-Mn bond revealed by several hybrid DFT calculations. Int J Quant Chem 113:525–541

    Google Scholar 

  • Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller F, Koroidov S, Brewster AS, …, Yano J (2016) Structure of photosystem II and substrate binding at room temperature. Nature 540:453–457

    Google Scholar 

  • Zaharieva I, Chernev P, Berggren G, Anderlund M, Styring S, Dau H, Haumann M (2016) Room-temperature energy-sampling Kβ X-ray emission spectroscopy of the Mn4Ca complex of photosynthesis reveals three manganese-centered oxidation steps and suggests a coordination change prior to O2 formation. Biochemistry 55:4197–4211

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert Stranger .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Stranger, R., Petrie, S., Terrett, R., Pace, R.J. (2021). On the Nature of the Functional S-States in the Oxygen Evolving Centre of Photosystem II—What Computational Chemistry Reveals About the Water Splitting Mechanism. In: Shen, JR., Satoh, K., Allakhverdiev, S.I. (eds) Photosynthesis: Molecular Approaches to Solar Energy Conversion. Advances in Photosynthesis and Respiration, vol 47. Springer, Cham. https://doi.org/10.1007/978-3-030-67407-6_3

Download citation

Publish with us

Policies and ethics