Solution structure of monomeric and trimeric photosystem I of Thermosynechococcus elongatus investigated by small-angle X-ray scattering

Abstract

The structure of monomeric and trimeric photosystem I (PS I) of Thermosynechococcus elongatus BP1 (T. elongatus) was investigated by small-angle X-ray scattering (SAXS). The scattering data reveal that the protein–detergent complexes possess radii of gyration of 58 and 78 Å in the cases of monomeric and trimeric PS I, respectively. The results also show that the samples are monodisperse, virtually free of aggregation, and contain empty detergent micelles. The shape of the protein–detergent complexes can be well approximated by elliptical cylinders with a height of 78 Å. Monomeric PS I in buffer solution exhibits minor and major radii of the elliptical cylinder of about 50 and 85 Å, respectively. In the case of trimeric PS I, both radii are equal to about 110 Å. The latter model can be shown to accommodate three elliptical cylinders equal to those describing monomeric PS I. A structure reconstitution also reveals that the protein–detergent complexes are larger than their respective crystal structures. The reconstituted structures are larger by about 20 Å mainly in the region of the hydrophobic surfaces of the monomeric and trimeric PS I complexes. This seeming contradiction can be resolved by the addition of a detergent belt constituted by a monolayer of dodecyl-β-D-maltoside molecules. Assuming a closest possible packing, a number of roughly 1024 and 1472 detergent molecules can be determined for monomeric and trimeric PS I, respectively. Taking the monolayer of detergent molecules into account, the solution structure can be almost perfectly modeled by the crystal structures of monomeric and trimeric PS I.

This is a preview of subscription content, access via your institution.

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

Abbreviations

β-DM:

Dodecyl-β-maltoside

C12E8:

Octaethylene glycol dodecyl ether

Chl:

Chlorophyll

HTG:

Heptyl-β-thioglucoside

PS I:

Photosystem I

PS II:

Photosystem II

PS Icc:

Core complex of Photosystem I

Rg :

Radius of gyration

SANS:

Small-angle neutron scattering

SAXS:

Small-angle X-ray scattering

pdb:

Protein data bank

IFT:

Indirect Fourier Transformation

References

  1. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635. doi:10.1038/nature02200

    CAS  Article  PubMed  Google Scholar 

  2. Cardoso MB, Smolensky D, Heller WT, O’Neill H (2009) Insight into the structure of light-harvesting complex II and Its stabilization in detergent solution. J Phys Chem B 113:16377–16383. doi:10.1021/Jp905050b

    CAS  Article  PubMed  Google Scholar 

  3. DeLano WL (2006) PyMOL molecular graphics system 0.99 edn., California U.S.A

  4. El-Mohsnawy E et al (2010) Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49:4740–4751. doi:10.1021/bi901807p

    CAS  Article  PubMed  Google Scholar 

  5. Feifel SC, Lokstein H, Hejazi M, Zouni A, Lisdat F (2015) Unidirectional photocurrent of photosystem I on π-system-modified graphene electrodes: nanobionic approaches for the construction of photobiohybrid systems. Langmuir 31:10590–10598. doi:10.1021/acs.langmuir.5b01625

    CAS  Article  PubMed  Google Scholar 

  6. Feigin LA, Svergun DI (1987) Structure analysis by small-angle x-ray and neutron scattering. Plenum Press, New York. doi:10.1007/978-1-4757-6624-0

    Book  Google Scholar 

  7. Franke D, Svergun DI (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Cryst 42:342–346. doi:10.1107/S0021889809000338

    CAS  Article  Google Scholar 

  8. Golbeck JH (2006) Photosystem I, The light-driven plastocyanin:ferredoxin oxidoreductase vol 24. 1 edn. Springer Netherlands, Dordrecht. doi:10.1007/978-1-4020-4256-0

    Book  Google Scholar 

  9. Golub M, Irrgang K-D, Rusevich L, Pieper J (2015) Vibrational dynamics of plant light-harvesting complex LHC II investigated by quasi- and inelastic neutron scattering. EPJ Web Conf 83:1–4. doi:10.1051/epjconf/20158302004

    CAS  Article  Google Scholar 

  10. Gorka M, Schartner J, van der Est A, Rogner M, Golbeck JH (2014) Light-mediated hydrogen generation in Photosystem I: attachment of a naphthoquinone-molecular wire-Pt nanoparticle to the A1A and A1B sites. BioChemistry 53:2295–2306. doi:10.1021/bi500104r

    CAS  Article  PubMed  Google Scholar 

  11. Guinier A, Fournet G (1955) Small-angle scattering of X-rays. John Wiley and Sons, New York. doi:10.1002/pol.1956.120199326

    Google Scholar 

  12. Hammersley AP, Svensson SO, Hanfland M, Fitch AN, and Hausermann D (1996) Two-dimensional detector software: from real detector to idealised image of two-theta scan. High Pressure Res 14:235–248. doi:10.1080/08957959608201408

    Article  Google Scholar 

  13. Hellmich J et al (2014) Native-like photosystem II superstructure at 2.44 A resolution through detergent extraction from the protein crystal. Structure 22:1607–1615. doi:10.1016/j.str.2014.09.007

    CAS  Article  PubMed  Google Scholar 

  14. Jacques DA, Trewhella J (2010) Small-angle scattering for structural biology–expanding the frontier while avoiding the pitfalls. Protein Sci 19:642–657. doi:10.1002/pro.351

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411:909–917. doi:10.1038/35082000

    CAS  Article  PubMed  Google Scholar 

  16. Kern J, Loll B, Luneberg C, DiFiore D, Biesiadka J, Irrgang KD, Zouni A (2005) Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. BBA 1706:147–157. doi:10.1016/j.bbabio.2004.10.007

    CAS  PubMed  Google Scholar 

  17. Kikhney AG, Svergun DI (2015) A practical guide to small angle X-ray scattering (SAXS) of flexible and intrinsically disordered proteins. FEBS Lett 589:2570–2577. doi:10.1016/j.febslet.2015.08.027

    CAS  Article  PubMed  Google Scholar 

  18. Kirkensgaard JJK, Holm JK, Larsen JK, Posselt D (2009) Simulation of small-angle X-ray scattering from thylakoid membranes. J Appl Cryst 42:649–659. doi:10.1107/S0021889809017701

    CAS  Article  Google Scholar 

  19. Kline SR (2006) Reduction and analysis of SANS and USANS data using IGOR Pro. J Appl Cryst 39:895–900. doi:10.1107/S0021889806035059

    CAS  Article  Google Scholar 

  20. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI (2003) PRIMUS: a windows PC-based system for small-angle scattering data analysis. J Appl Cryst 36:1277–1282. doi:10.1107/S0021889803012779

    CAS  Article  Google Scholar 

  21. Kühn P, Pieper J, Kaminskaya O, Eckert HJ, Lechner RE, Shuvalov V, Renger G (2005) Reaction pattern of photosystem II: oxidative water cleavage and protein flexibility. Photosynth Res 84:317–323. doi:10.1007/s11120-004-7079-8

    Article  PubMed  Google Scholar 

  22. Le RK et al (2014) Analysis of the solution structure of Thermosynechococcus elongatus photosystem I in n-dodecyl-beta-D-maltoside using small-angle neutron scattering and molecular dynamics simulation. Arch Biochem Biophys 550–551:50–57. doi:10.1016/j.abb.2014.04.005

    Article  PubMed  Google Scholar 

  23. le Maire M, Champeil P, Moller JV (2000) Interaction of membrane proteins and lipids with solubilizing detergents. BBA 1508:86–111. doi:10.1016/S0304-4157(00)00010-1

    CAS  Article  PubMed  Google Scholar 

  24. Li Y et al. (2016) Characterization of red-shifted phycobilisomes isolated from the chlorophyll f-containing cyanobacterium Halomicronema hongdechloris. BBA 1857:107–114. doi:10.1016/j.bbabio.2015.10.009

    CAS  PubMed  Google Scholar 

  25. Liberton M, Page LE, O’Dell WB, O’Neill H, Mamontov E, Urban VS, Pakrasi HB (2013) Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. J Biol Chem 288:3632–3640. doi:10.1074/jbc.M112.416933

    CAS  Article  PubMed  Google Scholar 

  26. Mazor Y, Nataf D, Toporik H, Nelson N (2014) Crystal structures of virus-like photosystem I complexes from the mesophilic cyanobacterium Synechocystis PCC 6803. eLife 3:1–17. doi:10.7554/eLife.01496

    Article  Google Scholar 

  27. Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 A resolution. eLife 4:1–18. doi:10.7554/eLife.07433

    Article  Google Scholar 

  28. Mershin A et al. (2012) Self-assembled photosystem-I biophotovoltaics on nanostructured TiO(2)and ZnO. Sci Rep 2:234. doi:10.1038/srep00234

    Article  PubMed  PubMed Central  Google Scholar 

  29. Mo Y, Lee BK, Ankner JF, Becker JM, Heller WT (2008) Detergent-associated solution conformations of Helical and beta-Barrel Membrane proteins. J Phys Chem B 112:13349–13354. doi:10.1021/Jp801266r

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Moller JV, le Maire M (1993) Detergent binding as a measure of hydrophobic surface area of integral membrane proteins. J Biol Chem 268:18659–18672

    CAS  PubMed  Google Scholar 

  31. Müh F, Zouni A (2008) Micelle formation in the presence of photosystem I. BBA 1778:2298–2307. doi:10.1016/j.bbamem.2008.05.016

    Article  PubMed  Google Scholar 

  32. Nagy G et al (2011) Reversible membrane reorganizations during photosynthesis in vivo: revealed by small-angle neutron scattering. Biochem J 436:225–230. doi:10.1042/BJ20110180

    CAS  Article  PubMed  Google Scholar 

  33. Nagy G, Garab G, Pieper J (2014) Neutron scattering in photosynthesis research. In: Allakhverdiev S, Rubin AB, Shuvalov VA (eds) Contemporary Problems of Photosynthesis vol 1. Institute of Computer Science, Izhevsk, pp 69–121

  34. NanoStar. (2015) Brucker. https://www.bruker.com/products/X-ray-diffraction-and-elemental-analysis/X-ray-diffraction/nanostar/overview.html.

  35. Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565. doi:10.1146/annurev.arplant.57.032905.105350

    CAS  Article  PubMed  Google Scholar 

  36. Neugebauer JM (1990) Detergents: an overview. Methods Enzymol 182:239–253. doi:10.1016/0076-6879(90)82020-3

    CAS  Article  PubMed  Google Scholar 

  37. O’Neill H, Heller WT, Helton KE, Urban VS, Greenbaum E (2007) Small-angle X-ray scattering study of photosystem I-detergent complexes: implications for membrane protein crystallization. J Phys Chem B 111:4211–4219. doi:10.1021/jp067463x

    Article  PubMed  Google Scholar 

  38. Pebay-Peyroula E, Garavito RM, Rosenbusch JP, Zulauf M, Timmins PA (1995) Detergent structure in tetragonal crystals of OmpF porin. Structure 3:1051–1059. doi:10.1016/S0969-2126(01)00241-6

    CAS  Article  PubMed  Google Scholar 

  39. Pieper J, Renger G (2009) Protein dynamics investigated by neutron scattering. Photosynth Res 102:281–293. doi:10.1007/s11120-009-9480-9

    CAS  Article  PubMed  Google Scholar 

  40. Pieper J et al (1999) Effects of Aggregation on Trimeric Light-Harvesting Complex II of Green Plants: A Hole-Burning Study. J Phys Chem A 103:2422–2428. doi:10.1021/jp983958d

    CAS  Article  Google Scholar 

  41. Pieper J, Irrgang KD, Renger G, Lechner RE (2004) Density of vibrational states of the light-harvesting complex II of green plants studied by inelastic neutron scattering. J Phys Chem B 108:10556–10565. doi:10.1021/Jp049341f

    CAS  Article  Google Scholar 

  42. Pieper J, Trapp M, Skomorokhov A, Natkaniec I, Peters J, Renger G (2012) Temperature-dependent vibrational and conformational dynamics of photosystem II membrane fragments from spinach investigated by elastic and inelastic neutron scattering. BBA 1817:1213–1219. doi:10.1016/j.bbabio.2012.03.020

    CAS  PubMed  Google Scholar 

  43. Pieper J, Rusevich L, Hauss T, Renger G (2015) Lamellar spacing of photosystem II membrane fragments upon dehydration studied by neutron membrane diffraction. Optofluid 2:36–40. doi:10.1515/optof-2015-0005

    Google Scholar 

  44. Saboe PO et al (2014) Two-dimensional protein crystals for solar energy conversion. Adv Mater 26:7064–7069. doi:10.1002/adma.201402375

    CAS  Article  PubMed  Google Scholar 

  45. Seddon AM, Curnow P, Booth PJ (2004) Membrane proteins, lipids and detergents: not just a soap opera. BBA 1666:105–117. doi:10.1016/j.bbamem.2004.04.011

    CAS  Article  PubMed  Google Scholar 

  46. Slowik D, Rossmann M, Konarev PV, Irrgang KD, Saenger W (2011) Structural investigation of PsbO from plant and cyanobacterial photosystem II. J Mol Biol 407:125–137. doi:10.1016/j.jmb.2011.01.013

    CAS  Article  PubMed  Google Scholar 

  47. Stieger KR et al (2016a) Engineering of supramolecular photoactive protein architectures: the defined co-assembly of photosystem I and cytochrome c using a nanoscaled DNA-matrix. Nanoscale 8:10695–10705. doi:10.1039/c6nr00097e

    CAS  Article  PubMed  Google Scholar 

  48. Stieger KR, Feifel SC, Lokstein H, Hejazi M, Zouni A, Lisdat F (2016b) Biohybrid architectures for efficient light-to-current conversion based on photosystem I within scalable 3D mesoporous electrodes. J Mater Chem A 24:17009–17017

  49. Svergun DI (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25:495–503. doi:10.1107/S0021889892001663

    Article  Google Scholar 

  50. Svergun DI, Barberato C, Koch MHJ (1995) CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules form atomic coordinates. J Appl Cryst 28:768–773. doi:10.1107/S0021889895007047

    CAS  Article  Google Scholar 

  51. Tang KH, Blankenship RE (2012) Neutron and light scattering studies of light-harvesting photosynthetic antenna complexes. Photosynth Res 111:205–217. doi:10.1007/s11120-011-9665-x

    CAS  Article  PubMed  Google Scholar 

  52. Tiede DM, Thiyagarjan P (1996) Characterization of photosynthetic supramolecular assemblies using small angle neutron scattering. In: Amesz J, Hoff AJ (eds) Biophysical Techniques in Photosynthesis, vol 3. Springer, Netherlands, pp 375–390. doi:10.1007/0-306-47960-5_23

    Google Scholar 

  53. Tiede DM, Littrell K, Marone PA, Zhang R, Thiyagarjan P (2000) Solution structure of a biological bimolecular electron transfer complex: characterization of the photosynthetic reaction center-cytochrome c2 protein complex by small angle neutron scattering. J Appl Cryst 33:560–564. doi:10.1107/S0021889800099891

    CAS  Article  Google Scholar 

  54. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473:55–60. doi:10.1038/nature09913

    CAS  Article  PubMed  Google Scholar 

  55. Vasil’ev S, Irrgang KD, Schrotter T, Bergmann A, Eichler HJ, Renger G (1997) Quenching of chlorophyll a fluorescence in the aggregates of LHCII: steady state fluorescence and picosecond relaxation kinetics. BioChemistry 36:7503–7512. doi:10.1021/bi9625253

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Financial Support provided by the Estonian Science Foundation (Grant No. 9453) and the Estonian Research Council (Grants IUT02-28 and SLOKT 12026 T) is gratefully acknowledged. J. P. is deeply indebted to the European Social Fund’s Internationalisation Programme DoRa for financial support. M.H., A.K., H.L., A.Z. gratefully acknowledge financial support by the Bundesministerium für Bildung and Forschung, BMBF, Germany (Biotechnologie 2010+, project: 031A154B). H.L. acknowledges GAČR grant No. P501/12/G005. We thank Dr. Joerg Fettke, University of Potsdam (Germany), for kindly providing access to the Bruker Microflex spectrometer.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jörg Pieper.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Golub, M., Hejazi, M., Kölsch, A. et al. Solution structure of monomeric and trimeric photosystem I of Thermosynechococcus elongatus investigated by small-angle X-ray scattering. Photosynth Res 133, 163–173 (2017). https://doi.org/10.1007/s11120-017-0342-6

Download citation

Keywords

  • Photosystem I
  • n-Dodecyl-β-D-maltoside
  • Detergent belt
  • Small-angle X-ray scattering