Skip to main content
SpringerLink
Log in

Proton Release Reaction of Tyrosine D in Photosystem II

  • Chapter
  • First Online:
Molecular Mechanisms of Proton-coupled Electron Transfer and Water Oxidation in Photosystem II

Part of the book series: Springer Theses ((Springer Theses))

  • 207 Accesses

Abstract

Photosystem II (PSII) has two symmetrically located redox-active tyrosine residues, YZ, which mediates electron transfer from the Mn cluster to P680 as a main electron mediator, and YD, which donates an electron to P680 as a peripheral electron donor. To understand these functional differences between YD and YZ, it is important to understand where the phenolic proton is released on its oxidation during the proton-coupled electron transfer process. Thus, to investigate the fate of the proton released from YD, we used Fourier-transform infrared (FTIR) spectroscopy. The proton detection method using FTIR spectroscopy, which was previously utilized for the S-state cycle in PSII (Suzuki et al., in J Am Chem Soc 131:7849 − 7857, [36]) was applied to YD measurements. In this method, a proton released into the bulk upon YD oxidation was monitored as the protonation reaction of Mes buffer detected by FTIR spectroscopy. Indeed, 0.84 ± 0.10 protons reach the bulk surface upon YD oxidation at one PSII center. Thus, the YD proton is not trapped by the neighboring histidine, D2-H189, but is rather released into the bulk from the protein. In contrast to YD, the YZ proton is released to the neighboring histidine, D1-H190, along a strong hydrogen bond. The difference between YZ and YD can be attributed to their hydrogen-bonded structures, which are controlled by the amino acid residues that have hydrogen-bonding with the Nπ atoms of the associated histidines (i.e., D1-N298 and D2-R294, which serve as hydrogen bond acceptors and donors, respectively). These results support the theoretical suggestion based on the X-ray structure of PSII (Saito et al., Proc Natl Acad Sci USA 110:7690–7695, [15]), and further explain the difference in the redox reaction rates between YZ and YD.

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 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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

  1. Diner BA, Britt RD (2005) The redox-active tyrosines YZ and YD. In: Wydrzynski TJ, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase. Springer, Dordrecht, The Netherlands, pp 207–233

    Google Scholar 

  2. Renger G, Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98:53–80

    Article  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. Haumann M, Liebisch P, Muller C, Barra M, Grabolle M, Dau H (2005) Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019–1021

    Article  ADS  Google Scholar 

  5. Noguchi T, Suzuki H, Tsuno M, Sugiura M, Kato C (2012) Time-resolved infrared detection of the proton and protein dynamics during photosynthetic oxygen evolution. Biochemistry 51:3205–3214

    Article  Google Scholar 

  6. Klauss A, Haumann M, Dau H (2015) Seven steps of alternating electron and proton transfer in photosystem II water oxidation traced by time-resolved photothermal beam deflection at improved sensitivity. J Phys Chem B 119:2677–2689

    Article  Google Scholar 

  7. Styring S, Sjöholm J, Mamedov F (2012) Two tyrosines that changed the world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim Biophys Acta 1817:76–87

    Article  Google Scholar 

  8. Vass I, Styring S (1991) pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30:830–839

    Article  Google Scholar 

  9. Styring S, Rutherford AW (1987) In the oxygen-evolving complex of Photosystem II the S0 state is oxidized to the S1 state by D+ (Signal II slow). Biochemistry 26:2401–2405

    Article  Google Scholar 

  10. Faller P, Debus RJ, Brettel K, Sugiura M, Rutherford AW, Boussac A (2001) Rapid formation of the stable tyrosyl radical in photosystem II. Proc Natl Acad Sci USA 98:14368–14373

    Article  ADS  Google Scholar 

  11. Buser CA, Thompson LK, Diner BA, Brudvig GW (1990) Electron-transfer reactions in manganese-depleted photosystem II. Biochemistry 29:8977–8985

    Article  Google Scholar 

  12. Rutherford AW, Boussac A, Faller P (2004) The stable tyrosyl radical in photosystem II: why D? Biochim Biophys Acta 1655:222–230

    Article  Google Scholar 

  13. Magnuson A, Rova M, Mamedov F, Fredriksson PO, Styring S (1999) The role of cytochrome b559 and tyrosineD in protection against photoinhibition during in vivo photoactivation of photosystem II. Biochim Biophys Acta 1411:180–191

    Article  Google Scholar 

  14. Ananyev GM, Sakiyan I, Diner BA, Dismukes GC (2002) A functional role for tyrosine-D in assembly of the inorganic core of the water oxidase complex of photosystem II and the kinetics of water oxidation. Biochemistry 41:974–980

    Article  Google Scholar 

  15. Saito K, Rutherford AW, Ishikita H (2013) Mechanism of tyrosine D oxidation in Photosystem II. Proc Natl Acad Sci USA 110:7690–7695

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  17. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342

    Article  Google Scholar 

  18. 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

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  20. Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, McIntosh L, Sithole I, Yocum CF (1989) Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28:9557–9565

    Article  Google Scholar 

  21. Faller P, Rutherford AW, Debus RJ (2002) Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry 41:12914–12920

    Article  Google Scholar 

  22. Faller P, Goussias C, Rutherford AW, Un S (2003) Resolving intermediates in biological proton-coupled electron transfer: a tyrosyl radical prior to proton movement. Proc Natl Acad Sci USA 100:8732–8735

    Article  ADS  Google Scholar 

  23. Berthomieu C, Hienerwadel R (2005) Vibrational spectroscopy to study the properties of redox-active tyrosines in photosystem II and other proteins. Biochim Biophys Acta 1707:51–66

    Article  Google Scholar 

  24. Havelius KG, Styring S (2007) pH dependent competition between YZ and YD in photosystem II probed by illumination at 5 K. Biochemistry 46:7865–7874

    Article  Google Scholar 

  25. Hammarström L, Styring S (2011) Proton-coupled electron transfer of tyrosines in Photosystem II and model systems for artificial photosynthesis: the role of a redox-active link between catalyst and photosensitizer. Energy Environ Sci 4:2379–2388

    Article  Google Scholar 

  26. Matsuoka H, Shen JR, Kawamori A, Nishiyama K, Ohba Y, Yamauchi S (2011) Proton-coupled electron-transfer processes in photosystem II probed by highly resolved g-anisotropy of redox-active tyrosine YZ. J Am Chem Soc 133:4655–4660

    Article  Google Scholar 

  27. Saito K, Shen JR, Ishida T, Ishikita H (2011) Short hydrogen bond between redox-active tyrosine YZ and D1-His190 in the photosystem II crystal structure. Biochemistry 50:9836–9844

    Article  Google Scholar 

  28. Chatterjee R, Coates CS, Milikisiyants S, Lee CI, Wagner A, Poluektov OG, Lakshmi KV (2013) High-frequency electron nuclear double-resonance spectroscopy studies of the mechanism of proton-coupled electron transfer at the tyrosine-D residue of photosystem II. Biochemistry 52:4781–4790

    Article  Google Scholar 

  29. Nakamura S, Nagao R, Takahashi R, Noguchi T (2014) Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II: relevance to the proton transfer mechanism of water oxidation. Biochemistry 53:3131–3144

    Article  Google Scholar 

  30. Ahlbrink R, Haumann M, Cherepanov D, Bogershausen O, Mulkidjanian A, Junge W (1998) Function of tyrosine Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry 37:1131–1142

    Article  Google Scholar 

  31. Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ (1999) Role of D1-His190 in the proton-coupled oxidation of tyrosine YZ in manganese-depleted photosystem II. Biochemistry 38:11851–11865

    Article  Google Scholar 

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

    Article  Google Scholar 

  33. Rappaport F, Boussac A, Force DA, Peloquin J, Brynda M, Sugiura M, Un S, Britt RD, Diner BA (2009) Probing the coupling between proton and electron transfer in photosystem II core complexes containing a 3-fluorotyrosine. J Am Chem Soc 131:4425–4433

    Article  Google Scholar 

  34. Manna P, LoBrutto R, Eijckelhoff C, Dekker JP, Vermaas W (1998) Role of Arg180 of the D2 protein in photosystem II structure and function. Eur J Biochem 251:142–154

    Article  Google Scholar 

  35. Hienerwadel R, Diner BA, Berthomieu C (2008) Molecular origin of the pH dependence of tyrosine D oxidation kinetics and radical stability in photosystem II. Biochim Biophys Acta 1777:525–531

    Article  Google Scholar 

  36. Suzuki H, Sugiura M, Noguchi T (2009) Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy. J Am Chem Soc 131:7849–7857

    Article  Google Scholar 

  37. Iwai M, Suzuki T, Kamiyama A, Sakurai I, Dohmae N, Inoue Y, Ikeuchi M (2010) The PsbK subunit is required for the stable assembly and stability of other small subunits in the PSII complex in the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. Plant Cell Physiol 51:554–560

    Article  Google Scholar 

  38. Hienerwadel R, Berthomieu C (1995) Bicarbonate binding to the non-heme iron of photosystem II investigated by Fourier transform infrared difference spectroscopy and 13C-labeled bicarbonate. Biochemistry 34:16288–16297

    Article  Google Scholar 

  39. Noguchi T, Inoue Y (1995) Identification of Fourier transform infrared signals from the non-heme iron in photosystem II. J Biochem 118:9–12

    Article  Google Scholar 

  40. Berthomieu C, Hienerwadel R (2001) Iron coordination in photosystem II: interaction between bicarbonate and the QB pocket studied by Fourier transform infrared spectroscopy. Biochemistry 40:4044–4052

    Article  Google Scholar 

  41. Takahashi R, Sugiura M, Noguchi T (2007) Water molecules coupled to the redox-active tyrosine YD in photosystem II as detected by FTIR spectroscopy. Biochemistry 46:14245–14249

    Article  Google Scholar 

  42. Noguchi T, Sugiura M (2002) FTIR detection of water reactions during the flash-induced S-state cycle of the photosynthetic water-oxidizing complex. Biochemistry 41:15706–15712

    Article  Google Scholar 

  43. Hienerwadel R, Boussac A, Breton J, Berthomieu C (1996) Fourier transform infrared difference study of tyrosineD oxidation and plastoquinone QA reduction in photosystem II. Biochemistry 35:15447–15460

    Article  Google Scholar 

  44. Hienerwadel R, Boussac A, Breton J, Diner BA, Berthomieu C (1997) Fourier transform infrared difference spectroscopy of photosystem II tyrosine D using site-directed mutagenesis and specific isotope labeling. Biochemistry 36:14712–14723

    Article  Google Scholar 

  45. Hienerwadel R, Gourion-Arsiquaud S, Ballottari M, Bassi R, Diner BA, Berthomieu C (2005) Formate binding near the redox-active tyrosineD in photosystem II: consequences on the properties of tyrD. Photosynth Res 84:139–144

    Article  Google Scholar 

  46. Noguchi T, Inoue Y, Tang XS (1997) Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry 36:14705–14711

    Article  Google Scholar 

  47. Chu H-A, Hillier W, Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide of photosystem II is ligated to the manganese ion that undergoes oxidation during the S1 to S2 transition: An isotope-edited FTIR study. Biochemistry 43:3152–3166

    Article  Google Scholar 

  48. Takahashi R, Noguchi T (2007) Criteria for determining the hydrogen-bond structures of a tyrosine side chain by Fourier transform infrared spectroscopy: density functional theory analyses of model hydrogen-bonded complexes of p-cresol. J Phys Chem B 111:13833–13844

    Article  Google Scholar 

  49. Tommos C, Davidsson L, Svensson B, Madsen C, Vermaas W, Styring S (1993) Modified EPR spectra of the tyrosineD radical in photosystem II in site-directed mutants of Synechocystis sp. PCC 6803: identification of side chains in the immediate vicinity of tyrosineD on the D2 protein. Biochemistry 32:5436–5441

    Article  Google Scholar 

  50. Tang XS, Chisholm DA, Dismukes GC, Brudvig GW, Diner BA (1993) Spectroscopic evidence from site-directed mutants of Synechocystis PCC6803 in favor of a close interaction between histidine 189 and redox-active tyrosine 160, both of polypeptide D2 of the photosystem II reaction center. Biochemistry 32:13742–13748

    Article  Google Scholar 

  51. Kessen S, Teutloff C, Kern J, Zouni A, Bittl R (2010) High-Field 2H-mims-ENDOR spectroscopy on PSII single crystals: Hydrogen bonding of Y•D. ChemPhysChem 11:1275–1282

    Article  Google Scholar 

  52. Sjöholm J, Mamedov F, Styring S (2014) Spectroscopic evidence for a redox-controlled proton gate at tyrosine D in Photosystem II. Biochemistry 53:5721–5723

    Article  Google Scholar 

  53. Boussac A, Etienne AL (1984) Midpoint potential of signal-II (slow) in tris-washed photosystem-II particles. Biochim Biophys Acta 766:576–581

    Article  Google Scholar 

  54. Metz JG, Nixon PJ, Rogner M, Brudvig GW, Diner BA (1989) Directed alteration of the D1 polypeptide of photosystem II: Evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron-donor, P680. Biochemistry 28:6960–6969

    Article  Google Scholar 

  55. Ishikita H, Knapp EW (2006) Function of redox-active tyrosine in photosystem II. Biophys J 90:3886–3896

    Article  Google Scholar 

  56. Nakamura S, Noguchi T (2015) Infrared detection of a proton released from tyrosine YD to the bulk upon its photo-oxidation in photosystem II. Biochemistry 54:5045–5053

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemical Sciences “A. Rossi Fanelli”, University of Rome “Sapienza”, Rome, Italy

    Dr. Shin Nakamura

Authors
  1. Dr. Shin Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shin Nakamura .

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

Nakamura, S. (2020). Proton Release Reaction of Tyrosine D in Photosystem II. In: Molecular Mechanisms of Proton-coupled Electron Transfer and Water Oxidation in Photosystem II. Springer Theses. Springer, Singapore. https://doi.org/10.1007/978-981-15-1584-2_3

Download citation

Publish with us

Policies and ethics

Search

Navigation