Skip to main content
SpringerLink
Log in

The study of conformational changes in photosystem II during a charge separation

  • Original Paper
  • Published:
Journal of Molecular Modeling Aims and scope Submit manuscript

Abstract

Photosystem II (PSII) is a multi-subunit pigment-protein complex and is one of several protein assemblies that function cooperatively in photosynthesis in plants and cyanobacteria. As more structural data on PSII become available, new questions arise concerning the nature of the charge separation in PSII reaction center (RC). The crystal structure of PSII RC from cyanobacteria Thermosynechococcus vulcanus was selected for the computational study of conformational changes in photosystem II associated to the charge separation process. The parameterization of cofactors and lipids for classical MD simulation with Amber force field was performed. The parametrized complex of PSII was embedded in the lipid membrane for MD simulation with Amber in Gromacs. The conformational behavior of protein and the cofactors directly involved in the charge separation were studied by MD simulations and QM/MM calculations. This study identified the most likely mechanism of the proton-coupled reduction of plastoquinone QB. After the charge separation and the first electron transfer to QB, the system undergoes conformational change allowing the first proton transfer to QB− mediated via Ser264. After the second electron transfer to QBH, the system again adopts conformation allowing the second proton transfer to QBH−. The reduced QBH2 would then leave the binding pocket.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

PQ:

Plastoquinone

PSII:

Photosystem II

Pheo:

Pheophytin

POPC:

1-Palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine

Chl:

Chlorophyll

RC:

Reaction center

Cyt:

Cytochrome

QA :

Plastoquinone A

QB :

Plastoquionone B

DGDG:

Digalactosyl-diacylglycerol

SQDG:

Sulfoquinovosyl-diacylglycerol

MGDG:

Monogalactosyl-diacylglycerol

PG:

1,2-Dipalmitoyl-phosphatidyl-glycerol

uQ:

Ubiquinone

bRC:

Bacterial reaction center

References

  1. Vermaas W (1998) An introduction to photosynthesis and its applications The World & I: 158–165

  2. Wydrzynski T, Satoh S (2005) Photosystem II: the light-driven water: plastoquinone oxidoreductase, Springer, Dordrecht

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

    CAS  PubMed  Google Scholar 

  4. Müh F, Glöckner C, Hellmich J, Zouni A (2012) Light-induced quinone reduction in photosystem II. Biochim Biophys Acta 1817:44–65

    PubMed  Google Scholar 

  5. Zheleva D, Hankamer B, Barber J (1996) Heterogeneity and pigment composition of isolated photosystem II reaction centers. Biochemistry 35:15074–15079

    CAS  PubMed  Google Scholar 

  6. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0A resolution structure of photosystem II. Nature 438:1040–1044

    CAS  PubMed  Google Scholar 

  7. Biesiadka J, Loll B, Kern J, Irrgang KD, Zouni A (2004) Crystal structure of cyanobacterial photosystem II at 3.2 angstrom resolution: a closer look at the Mn-cluster. Phys Chem Chem Phys 6:4733–4736

    CAS  Google Scholar 

  8. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture ofthephotosyntheticoxygen-evolvingcenter. Science 303:1831–1838

    CAS  PubMed  Google Scholar 

  9. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-A resolution. Proc Natl Acad Sci U S A 100(1):98–103

    CAS  PubMed  Google Scholar 

  10. Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongates at 3.8 Å resolution. Nature 409:739–743

    CAS  PubMed  Google Scholar 

  11. Tanaka A, Fukushima Y, Kamiya N (2017) Two different structures of the oxygen-evolving complex in the same polypeptide frameworks of photosystem II. J Am Chem Soc 139(5):1718–1721

    CAS  PubMed  Google Scholar 

  12. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 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

    CAS  PubMed  Google Scholar 

  14. Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74

    CAS  PubMed  Google Scholar 

  15. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007) Lipids in photosystem II: interactions with protein and cofactors. Biochim Biophys Acta 1767:509–519

    CAS  PubMed  Google Scholar 

  16. Van Eerden FJ, Melo MN, Frederix PWJM, Periole X, Marrink SJ (2017) Exchange pathways of plastoquinone and plastoquinol in the photosystem II complex. Nat Commun 8:15214

    PubMed  PubMed Central  Google Scholar 

  17. Okamura MY, Paddock ML, Graige MS, Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458:148–163

    CAS  PubMed  Google Scholar 

  18. Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, Wang F, Zou H, Enami I, Miyano M, Shen JR (2016) Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem 291:5676–5687

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Krieger E, Koraimann G, Vriend G (2002) Increasing the precision of comparative models with YASARA NOVA--a self-parameterizing force field. Proteins 47:393–402

    CAS  PubMed  Google Scholar 

  20. Zayats V, Stockner T, Pandey SK, Wörz K, Ettrich R, Ludwig J (2015) A refined atomic scale model of the Saccharomyces cerevisiae K(+)-translocation protein Trk1p combined with experimental evidence confirms the role of selectivity filter glycines and other key residues. Biochim Biophys Acta 1848:1183–1195

    CAS  PubMed  Google Scholar 

  21. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJC (2005) GROMACS: fast, flexible, and free. J Comput Chem 26:1701–1718

    Google Scholar 

  22. Berendsen HJC, van der Spoel D, van Drunen R (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput Phys Commun 91:43–56

    Article  CAS  Google Scholar 

  23. Pronk S, Pall S, Schulz R, Larsson P, Bjelkmar P et al (2013) GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics 29:845–854

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65:712–725

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472

    CAS  Google Scholar 

  26. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an N•log(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092

    CAS  Google Scholar 

  27. Humphrey W, Dalke A, Schulten K (1996) VMD - visual molecular dynamics. J Molec Graphics 14:33–38

    CAS  Google Scholar 

  28. Zhang L, Silva DA, Yan Y, Huang X (2012) Force field development for cofactors in the photosystem II. J Comput Chem 33:1969–1980

    CAS  PubMed  Google Scholar 

  29. Jämbeck JPM, Lyubartsev AP (2012) Derivation and systematic validation of a refined all-atom force field for phosphatidylcholine lipids. J Phys Chem B 116:3164–3179

    PubMed  PubMed Central  Google Scholar 

  30. Bayly CI, Cieplak P, Cornell W, Kollman PA (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J Phys Chem 97:10269–10280

    CAS  Google Scholar 

  31. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Pople JA et al (2010) GAUSSIAN 09 (revision B.01). Gaussian, Wallingford

  32. Wang J, Wang W, Kollman PA, Case DA (2006) Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 25:247260

    Google Scholar 

  33. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general AMBER force field. J Comput Chem 2:1157–1174

    Google Scholar 

  34. Hub JS, de Groot BL, van der Spoel D (2010) g_wham—a free weighted histogram analysis implementation including robust error and autocorrelation estimates. J Chem Theory Comput 6:3713–3720

    CAS  Google Scholar 

  35. Small-Molecule Drug Discovery Suite 2015–1 (2015) QSite, version 6.6, Schrödinger, LLC, New York, NY

  36. Murphy RB, Philipp DM, Friesner RA (2000) A mixed quantum mechanics/molecular mechanics (QM/MM) method for large-scale modeling of chemistry in protein environments. J Comp Chem 21:1442–1457

    CAS  Google Scholar 

  37. Hasegawa K, Noguchi T (2014) Molecular interactions of the quinone electron acceptors Q(A), Q(B), and Q(C) in photosystem II as studied by the fragment molecular orbital method. Photosynth Res 120:113–123

  38. Kern J, Renger G (2007) Photosystem II: structure and mechanism of the water: plastoquinone oxidoreductase. Photosynth Res 94:183–202

    CAS  PubMed  Google Scholar 

  39. Balabin IA, Onuchic JN (2000) Dynamically controlled protein tunneling paths in photosynthetic reaction centers. Science. 290:114–117

    CAS  PubMed  Google Scholar 

  40. Nishioka H, Kimura A, Yamato T, Kawatsu T, Kakitani T (2005) Interference, fluctuation, and alternation of electron tunneling in protein media. 1. Two tunneling routes in photosynthetic reaction center alternate due to thermal fluctuation of protein conformation. J Phys Chem B 109(5):1978–1987

    CAS  PubMed  Google Scholar 

  41. Ishikita H, Knapp EW (2005) Control of quinone redox potentials in photosystem II: electron transfer and photoprotection. J Am Chem Soc 127:14714–14720

    CAS  PubMed  Google Scholar 

  42. Lambreva MD, Russo D, Polticelli F, Scognamiglio V, Antonacci A, Zobnina V, Campi G, Rea G (2014) Structure/function/dynamics of photosystem II plastoquinone binding sites. Curr Protein Pept Sci 15:285–295

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Broser M, Glöckner C, Gabdulkhakov A, Guskov A, Buchta J, Kern J, Müh F, Dau H, Saenger W, Zouni A (2011) Structural basis of cyanobacterial photosystem II inhibition by the herbicide terbutryn. J Biol Chem 286:15964–15972

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Graige MS, Paddock ML, Bruce JM, Feher G, Okamura MY (1996) Mechanism of proton-coupled electron transfer for quinone (Q B ) reduction in reaction centers of Rb. sphaeroides. J Am Chem Soc 118:9005–9016

    CAS  Google Scholar 

  45. Graige MS, Paddock ML, Feher G, Okamura MY (1999) Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: implications for the mechanism of electron and proton transfer in proteins. Biochemistry 38:11465–11473

    CAS  PubMed  Google Scholar 

  46. Graige MS, Feher G, Okamura MY (1998) Conformational gating of the electron transfer reaction QA- QB –> QAQB- in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay. Proc Natl Acad Sci U S A. 95:11679–11684

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Stowell MH, McPhillips TM, Rees DC, Soltis SM, Abresch E, Feher G (1997) Light-induced structural changes in photosynthetic reaction center: implications for mechanism of electron-proton transfer. Science. 276:812–816

    CAS  PubMed  Google Scholar 

  48. Baxter RH, Ponomarenko N, Srajer V, Pahl R, Moffat K, Norris JR (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center. Proc Natl Acad Sci U S A. 101:5982–5987

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Reifarth F, Renger G (1998) Indirect evidence for structural changes coupled with QB- formation in photosystem II. FEBS Lett. 428:123–126

    CAS  PubMed  Google Scholar 

  50. Alexov EG, Gunner MR (1999) Calculated protein and proton motions coupled to electron transfer: electron transfer from QA- to QB in bacterial photosynthetic reaction centers. Biochemistry 38:8253–8270

    CAS  PubMed  Google Scholar 

  51. Saito K, Rutherford AW, Ishikita H (2013) Mechanism of proton-coupled quinone reduction in photosystem II. Proc Natl Acad Sci U S A. 110:954–959

    CAS  PubMed  Google Scholar 

  52. Sundby C et al (1993) Effects on photosystem II function, photoinhibition, and plant performance of the spontaneous mutation of Serine-264 in the photosystem II reaction center D1 protein in triazine-resistant Brassica napus L. Plant Physiol. 103:105–113

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Chernyshev A, Cukierman S (2002) Thermodynamic view of activation energies of proton transfer in various gramicidin A channels. Biophys J 82:182–192

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Klauss A, Haumann M, Dau H (2012) Alternating electron and proton transfer steps in photosynthetic water oxidation. PNAS 109:16035–16040

    CAS  PubMed  Google Scholar 

  55. Cox N, Jin L, Jaszewski A, Smith PJ, Krausz E, Rutherford AW, Pace R (2009) The semiquinone–iron complex of photosystem II: structural insights from ESR and theoretical simulation; evidence that the native ligand to the non-heme iron is carbonate. Biophys J 97:2024–2033

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Ishikita H, Saito K (2013) Proton transfer reactions and hydrogen-bond networks in protein environments. J R Soc Interface 11:20130518

    PubMed  Google Scholar 

  57. Shevela D, Eaton-Rye JJ, Shen JR, Govindjee (2012) Photosystem II and the unique role of bicarbonate: a historical perspective. Biochim Biophys Acta 1817:1134–1151

    CAS  PubMed  Google Scholar 

  58. Xiong J, Subramaniam S, Govindjee (1996) Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center: implications for herbicide and bicarbonate binding. Protein Sci. 5:2054–2073

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Czech Science Foundation (project no GA15-12816S). Access to computing and storage facilities owned by parties and projects contributing to the National Grid Infrastructure MetaCentrum provided under the program “Projects of Large Research, Development, and Innovations Infrastructures” (CESNET LM2015042) is greatly appreciated.

Author information

Authors and Affiliations

  1. Center for Nanobiology and Structural Biology, Institute of Microbiology of the Czech Academy of Sciences, Zamek 136, 373 33, Nove Hrady, Czech Republic

    Natalia Kulik, Michal Kutý & David Řeha

  2. Institute of Chemistry, Faculty of Science, University of South Bohemia, Branisovska 1760, CZ-370 05, Ceske Budejovice, Czech Republic

    Michal Kutý

Authors
  1. Natalia Kulik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michal Kutý
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Řeha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David Řeha.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 2489 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kulik, N., Kutý, M. & Řeha, D. The study of conformational changes in photosystem II during a charge separation. J Mol Model 26, 75 (2020). https://doi.org/10.1007/s00894-020-4332-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00894-020-4332-9

Keywords

Search

Navigation