Photosynthesis Research

, Volume 102, Issue 2–3, pp 267–279 | Cite as

X-ray scattering combined with coordinate-based analyses for applications in natural and artificial photosynthesis

Review

Abstract

Advances in X-ray light sources and detectors have created opportunities for advancing our understanding of structure and structural dynamics for supramolecular assemblies in solution by combining X-ray scattering measurement with coordinate-based modeling methods. In this review the foundations for X-ray scattering are discussed and illustrated with selected examples demonstrating the ability to correlate solution X-ray scattering measurements to molecular structure, conformation, and dynamics. These approaches are anticipated to have a broad range of applications in natural and artificial photosynthesis by offering possibilities for structure resolution for dynamic supramolecular assemblies in solution that can not be fully addressed with crystallographic techniques, and for resolving fundamental mechanisms for solar energy conversion by mapping out structure in light-excited reaction states.

Keywords

X-ray scattering Photosynthesis Artificial photosynthesis Solution structure Supramolecular chemistry Molecular dynamics Structure-function 

Abbreviations

DNA

Deoxyribonucleic acid

PDF

Pair distribution function

MD

Molecular dynamics

NMR

Nuclear magnetic resonance

SAXS

Small angle X-ray scattering

WAXS

Wide angle X-ray scattering

Notes

Acknowledgments

This study was supported by the Office of Science, Basic Energy Sciences, U. S. Department of Energy under contract numbers DE-AC02-06CH11357 (D.M.T. and work at APS Sector 12), National Science Foundation IL-LSAMP grant HRD-0413000, and National Institutes of Health Grant 1SC2GM083717 (K.L.M.). The software program, solX, used for coordinated based X-ray scattering calculations is available by request to D.M.T. or X.Z.

References

  1. Bernadó P, Mylonas M, Petoukhov MV, Blackledge M, Svergun DI (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J Am Chem Soc 129:5656–5664CrossRefPubMedGoogle Scholar
  2. Bernstein FC, Koetzle TF, Williams GJB, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The protein data bank: a computer-based archival file for macromolecular structures. J Mol Biol 112:535–542CrossRefPubMedGoogle Scholar
  3. Borgstahl GEO, Williams DR, Getzoff ED (1995) 1.4 angstrom structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active site, and chromophore. Biochemistry 34:6278–6287CrossRefPubMedGoogle Scholar
  4. Cammarata M, Levantino M, Schotte F, Anfinrud PA, Ewald F, Choi J, Cupane A, Wulff M, Ihee H (2008) Tracking the structural dynamics of proteins in solution using time-resolved wide-angle X-ray scattering (vol 5, pg 881, 2008). Nat Methods 5:988CrossRefGoogle Scholar
  5. Christen M, van Gunsteren WF (2008) On searching in, sampling of, and dynamically moving through conformational space of biomolecular systems: a review. J Comput Chem 29:157–166CrossRefPubMedGoogle Scholar
  6. Ducruix A, Guilloteau JP, Ries-Kautt M, Tardieu A (1996) Protein interactions as seen by solution X-ray scattering prior to crystallogenesis. J Cryst Growth 168:28–39CrossRefGoogle Scholar
  7. Fedorov BA, Denesyuk AI (1978) Large-angle X-ray diffuse scattering, a new method for investigating changes in the conformation of globular proteins in solution. J Appl Cryst 11:473–477CrossRefGoogle Scholar
  8. Fischetti RF, Rodi DJ, Gore DB, Makowski L (2004) Wide-angle X-ray solution scattering as a probe of ligand-induced conformational changes in proteins. Chem Biol 11:1431–1443CrossRefPubMedGoogle Scholar
  9. Fraser RDB, MacRae TP, Suzuki E (1978) An improved method for calculating the contribution of solvent to the X-ray diffraction pattern of biological molecules. J Appl Crystallogr 11:693–694CrossRefGoogle Scholar
  10. Gabel F, Simon B, Sattler M (2006) A target function for quaternary structural refinement from small angle scattering and NMR orientational restraints. Eur Biophys J 35:313–327CrossRefPubMedGoogle Scholar
  11. Genick UK, Borgstahl GEO, Ng K, Ren Z, Pradervand C, Burke PM, Srajer V, Teng TY, Schildkamp W, McRee DE, Moffat K, Getzoff ED (1997) Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science 275:1471–1475CrossRefPubMedGoogle Scholar
  12. Grishaev A, Wu J, Trewhella J, Bax A (2005) Refinement of multidomain protein structures by combination of solution small-angle X-ray scattering and NMR data. J Am Chem Soc 127:16621–16628CrossRefPubMedGoogle Scholar
  13. Grishaev A, Ying J, Canny MD, Pardi A, Bax A (2008) Solution structure of tRNAVal from refinement of homology model against residual dipolar coupling and SAXS data. J Biomol NMR 42:99–109CrossRefPubMedGoogle Scholar
  14. Guinier A, Fournet G (1955) Small angle scattering of X-rays. Wiley, New YorkGoogle Scholar
  15. Gust D, Moore TA, Moore AL (2001) Mimicking photosynthetic solar energy transduction. Acc Chem Res 34:40–48CrossRefPubMedGoogle Scholar
  16. Hamelberg D, de Oliveira CAF, McCammon JA (2007) Sampling of slow diffusive conformational transitions with accelerated molecular dynamics. J Chem Phys 127:155102-1–155102-9CrossRefGoogle Scholar
  17. Hellemans A (1997) X-rays find new ways to shine. Science 277:1214–1215CrossRefGoogle Scholar
  18. Hirai M, Koizumi M, Hayakawa T, Takahashi H, Abe S, Hirai H, Miura K, Inoue K (2004) Hierarchical map of protein unfolding and refolding at thermal equilibrium revealed by wide-angle X-ray scattering. Biochemistry 43:9036–9049CrossRefPubMedGoogle Scholar
  19. Howard AE, Kollman PA (1988) An analysis of current methodologies for conformational searching of complex molecules. J Med Chem 31:1669–1675CrossRefPubMedGoogle Scholar
  20. Ihee H, Lorenc M, Kim TK, Kong QY, Cammarata M, Lee JH, Bratos S, Wulff M (2005) Ultrafast X-ray diffraction of transient molecular structures in solution. Science 309:1223–1227CrossRefPubMedGoogle Scholar
  21. Kamikubo H, Shimizu N, Harigai M, Yamazaki Y, Imamoto Y, Kataoka M (2007) Characterization of the solution structure of the M intermediate of photoactive yellow protein using high-angle solution X-ray scattering. Biophys J 92:3633–3642CrossRefPubMedGoogle Scholar
  22. Kim TK, Zuo X, Tiede DM, Ihee H (2004) Exploring fine structures of photoactive yellow protein in solution using wide-angle X-ray scattering. Bull Korean Chem Soc 25:1676–1680CrossRefGoogle Scholar
  23. Kim SJ, Dumont C, Gruebele M (2008) Simulation-based fitting of protein-protein interaction potentials to SAXS experiments. Biophys J 94:4924–4931CrossRefPubMedGoogle Scholar
  24. Koch MHJ (2006) X-ray scattering of non-crystalline biological systems using synchrotron radiation. Chem Soc Rev 35:123–133CrossRefPubMedGoogle Scholar
  25. Kojima M, Timchenko AA, Higo J, Ito K, Kihara H, Takakhashi K (2004) Structural refinement by restrained molecular-dynamics algorithm with small-angle X-ray scattering constraints for a biomolecule. J Appl Cryst 37:103–109CrossRefGoogle Scholar
  26. Kojima M, Kezuka Y, Nonaka T, Hiragi Y, Watanabe T, Kimura K, Takahashi K, Yanagi S, Kihara H (2008) SaxsMDView: a three-dimensional graphics program for displaying force vectors. J Synchrot Radiat 15:535–537CrossRefGoogle Scholar
  27. Kuszewski J, Schwieters C, Clore GM (2001) Improving the accuracy of NMR structures of DNA by means of a database potential of mean force describing base-base positional interactions. J Am Chem Soc 123:3903–3918CrossRefPubMedGoogle Scholar
  28. Lee SJ, Mulfort KL, O’Donnell JL, Zuo X, Goshe AJ, Nguyen ST, Hupp JT, Tiede DM (2006) Supramolecular porphyrinic prisms: coordinative assembly and preliminary solution-phase X-ray structural characterization. Chem Commun 458:1–4583Google Scholar
  29. Lee D, Walsh JD, Yu P, Markus MA, Choli-Papadopoulou T, Schwieters CD, Krueger S, Draper DE, Wang YX (2007) The structure of free L11 and functional dynamics of L11 in free, L11-rRNA(58 nt) binary and L11-rRNA(58 nt)-thiostrepton ternary complexes. J Mol Biol 367:1007–1022CrossRefPubMedGoogle Scholar
  30. Lee SJ, Mulfort KL, Zuo X, Goshe AJ, Wesson PJ, Nguyen ST, Hupp JT, Tiede DM (2008) Coordinative self-assembly and solution-phase X-ray structural characterization of cavity-tailored porphyrin boxes. J Am Chem Soc 130:836–838CrossRefPubMedGoogle Scholar
  31. Lipfert J, Doniach S (2007) Small-angle X-ray scattering from RNA, proteins, and protein complexes. Annu Rev Biophys Biomol Struct 36:307–327CrossRefPubMedGoogle Scholar
  32. Makowski L, Rodi DJ, Mandava S, Devarapalli S, Fischetti RF (2008) Characterization of protein fold by wide-angle X-ray solution scattering. J Mol Biol 383:731–744CrossRefPubMedGoogle Scholar
  33. Mardis KL, Sutton HM, Zuo XB, Lindsey JS, Tiede DM (2009) Solution-state conformational ensemble of a hexameric porphyrin array characterized using molecular dynamics and X-ray scattering. J Phys Chem A 113:2516–2523CrossRefPubMedGoogle Scholar
  34. Markwick PRL, Bouvignies G, Blackledge M (2007) Exploring multiple timescale motions in protein GB3 using accelerated molecular dynamics and NMR spectroscopy. J Amer Chem Soc 129:4724–4730CrossRefGoogle Scholar
  35. Marone PA, Thiyagarajan P, Wagner AM, Tiede DM (1998) The association state of a detergent-solubilized membrane protein measured during crystal nucleation and growth by small-angle neutron scattering. J Cryst Growth 191:811–819CrossRefGoogle Scholar
  36. Marrink SJ, de Vries AH, Mark AE (2004) Coarse Grained Model for Semiquantitative Lipid Simulations. J. Phys. Chem. B 108:750–760CrossRefGoogle Scholar
  37. Megyes T, Jude H, Grósz T, Bakó I, Radnai T, Tárkányi G, Pálinkás G, Stang PJ (2005) X-ray diffraction and DOSY-NMR characterization of self-assembled supramolecular metallocyclic species in solution. J Am Chem Soc 127:10731–10738CrossRefPubMedGoogle Scholar
  38. Megyes T, Balint S, Bako I, Grosz T, Palinkas G (2008) Complete structural characterization of metallacyclic complexes in solution-phase using simultaneously X-ray diffraction and molecular dynamics simulation. J Am Chem Soc 130:9206–9209CrossRefPubMedGoogle Scholar
  39. O’Donnell JL, Zuo X, Goshe AJ, Sarkisov L, Snurr RQ, Hupp JT, Tiede DM (2007) Solution-phase structural characterization of supramolecular assemblies by molecular diffraction. J Am Chem Soc 129:1578–1585CrossRefPubMedGoogle Scholar
  40. Petoukhov MV, Svergun DI (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J 89:1237–1250CrossRefPubMedGoogle Scholar
  41. Petoukhov MV, Eady NAJ, Brown KA, Svergun DI (2002) Addition of missing loops and domains to protein models by X-ray solution scattering. Biophys J 83:3113–3125CrossRefPubMedGoogle Scholar
  42. Philip AF, Eisenman KT, Papadantonakis GA, Hoff WD (2008) Functional tuning of photoactive yellow protein by active site residue 46. Biochemistry 47:13800–13810CrossRefPubMedGoogle Scholar
  43. Plech A, Wulff M, Bratos S, Mirloup F, Vuilleumier R, Schotte F, Anfinrud PA (2004) Visualizing chemical reactions in solution by picosecond X-ray diffraction. Phys Rev Lett 92:125505-1–125505-5Google Scholar
  44. Pontius J, Richelle J, Wodak J (1996) Deviations from standard atomic volumes as a quality measure for protein crystal structures. J Mol Biol 264:121–136CrossRefPubMedGoogle Scholar
  45. Putnam CD, Hammel M, Hura GL, Tainer JA (2007) X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 40:191–285PubMedGoogle Scholar
  46. Riekel C, Bosecke P, Diat O, Engstrom P (1996) New opportunities in small-angle X-ray scattering and wide-angle X-ray scattering at a third generation synchrotron radiation source. J Mol Struct 383:291–302CrossRefGoogle Scholar
  47. Schatz GC (2007) Using theory and computation to model nanoscale properties. Proc Natl Acad Sci USA 104:6885–6892CrossRefPubMedGoogle Scholar
  48. Schwieters CD, Clore GM (2006) A physical picture of atomic motions within the Dickerson DNA dodecamer in solution derived from joint ensemble refinement against NMR and large-angle X-ray scattering data. Biochemistry 46:1152–1166CrossRefGoogle Scholar
  49. Seifert S, Winans RE, Tiede DM, Thiyagarajan P (2000) Design and performance of an ASAXS instrument at the advanced photon source. J Appl Cryst 33:782–784CrossRefGoogle Scholar
  50. Semenyuk AV, Svergun DI (1991) GNOM—a program package for small-angle scattering data processing. J Appl Cryst 24:537–540CrossRefGoogle Scholar
  51. Sivaramakrishnan S, Spink BJ, Sim AYL, Doniach S, Spudich JA (2008) Dynamic charge interactions create surprising rigidity in the ER/K alpha-helical protein motif. Proc Natl Acad Sci USA 105:13356–13361CrossRefPubMedGoogle Scholar
  52. Svensson B, Tiede DM, Barry BA (2002) Small-angle X-ray scattering studies of the manganese stabilizing subunit in photosystem II. J Phys Chem B 106:8485–8488CrossRefGoogle Scholar
  53. Svensson B, Tiede DM, Nelson DR, Barry BA (2004) Structural studies of the manganese-stabilizing subunit in photosystem II. Biophys J 86:1807–1812CrossRefPubMedGoogle Scholar
  54. Svergun DI, Koch MHJ (2003) Small-angle scattering studies of biological macromolecules in solution. Rep Prog Phys 66:1735–1782CrossRefGoogle Scholar
  55. Svergun D, Barberato C, Koch MHJ (1995) CRYSOL—a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Cryst 28:768–773CrossRefGoogle Scholar
  56. Svergun DI, Petoukhov MV, Koch MHJ (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80:2946–2953CrossRefPubMedGoogle Scholar
  57. Tama F, Brooks CL (2006) SYMMETRY, FORM, AND SHAPE: guiding principles for robustness in macromolecular machines. Ann Rev Biophys Biomol Struct 35:115–133CrossRefGoogle Scholar
  58. Tiede DM, Littrell K, Marone PA, Zhang R, Thiyagarajan 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 Crystallogr 33:560–564CrossRefGoogle Scholar
  59. Tiede DM, Zhang R, Seifert S (2002) Protein conformations explored by difference high-angle solution X-ray scattering: oxidation state and temperature dependent changes in cytochrome c. Biochemistry 41:6605–6614CrossRefPubMedGoogle Scholar
  60. Tiede DM, Zhang R, Chen LX, Yu L, Lindsey JS (2004) Structural characterization of modular supramolecular architectures in solution. J Am Chem Soc 126:14054–14062CrossRefPubMedGoogle Scholar
  61. Tozzini V (2005) Coarse-grained models for proteins. Theory simul/Macromol assemblages 15:144–150Google Scholar
  62. Tsuruta H, Irving TC (2008) Experimental approaches for solution X-ray scattering and fiber diffraction. Curr Opinion Struct Biol 18:601–608CrossRefGoogle Scholar
  63. van Gunsteren WF, Bakowies D, Baron R, Chandrasekhar I, Christen M, Daura X, Gee P, Geerke DP, Glättli A, Hünenberger PH, Kastenholz MA, Oostenbrink C, Schenk M, Trzesniak D, van der Vegt NFA, Yu HB (2006) Biomolecular modeling: goals, problems, perspectives. Angew Chem Int Edit 45:4064–4092CrossRefGoogle Scholar
  64. Vaughan PA, Sturdivant JH, Pauling L (1950) The determination of the structures of complex molecules and ions from X-ray diffraction by their solutions: the structures of the groups PtBr6− −, PtCl6− −, Nb6Cl12 ++, TaBr12 ++, and Ta6Cl12 ++. J Am Chem Soc 72:5477–5486CrossRefGoogle Scholar
  65. Vengadesan K, Gautham N (2005) A new conformational search technique and its applications. Curr Sci 88:1759Google Scholar
  66. Vigil D, Gallagher SC, Trewhella J, Garcia AE (2001) Functional dynamics of the hydrophobic cleft in the N-domain of calmodulin. Biophys J 80:2082–2092CrossRefPubMedGoogle Scholar
  67. von Ossowski I, Eaton JT, Czjzek M, Perkins SJ, Frandsen TP, Schulein M, Panine P, Henrissat B, Receveur-Brechot V (2005) Protein disorder: conformational distribution of the flexible linker in a chimeric double cellulase. Biophys J 88:2823–2832CrossRefGoogle Scholar
  68. Warren BE (1990) X-ray diffraction. Dover Publications Inc., New YorkGoogle Scholar
  69. Wasielewski MR (2006) Energy, charge, and spin transport in molecules and self-assembled nanostructures inspired by photosynthesis. J Org Chem 71:5051–5066CrossRefPubMedGoogle Scholar
  70. Winick H (1998) Synchrotron radiation sources—Present capabilities and future directions. J Synchrot Radiat 5:168–175CrossRefGoogle Scholar
  71. Xie AH, Kelemen L, Hendriks J, White BJ, Hellingwerf KJ, Hoff WD (2001) Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation. Biochemistry 40:1510–1517CrossRefPubMedGoogle Scholar
  72. Yang L, Grubb MP, Gao YQ (2007) Application of the accelerated molecular dynamics simulations to the folding of a small protein. J Chem Phys 126:125102-1–125102-7Google Scholar
  73. Yeremenko S, van Stokkum IHM, Moffat K, Hellingwerf KJ (2006) Influence of the crystalline state on photoinduced dynamics of photoactive yellow protein studied by ultraviolet-visible transient absorption spectroscopy. Biophys J 90:4224–4235CrossRefPubMedGoogle Scholar
  74. Zhang LY, Friesner RA (1998) Ab initio calculation of electronic coupling in the photosynthetic reaction center. Proc Natl Acad Sci USA 95:13603–13605CrossRefPubMedGoogle Scholar
  75. Zuo X, Tiede DM (2005) Resolving conflicting crystallographic and NMR models for solution-state DNA with solution X-ray diffraction. J Am Chem Soc 127:16–17CrossRefPubMedGoogle Scholar
  76. Zuo X, Cui G, Mertz KM, Zhang L, Lewis FD, Tiede DM (2006) X-ray diffraction “fingerprinting” of DNA structure in solution for quantitative evaluation of molecular dynamics simulation. Proc Natl Acad Sci USA 103:3534–3539CrossRefPubMedGoogle Scholar
  77. Zuo X, Wang J, Foster TR, Schwieters CD, Tiede DM, Butcher SE, Wang Y-X (2008) Global architecture and interface: refining a RNA:RNA complex structure using solution X-ray scattering data. J Am Chem Soc 130:3292–3293CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • David M. Tiede
    • 1
  • Kristy L. Mardis
    • 2
  • Xiaobing Zuo
    • 3
  1. 1.Chemical Sciences and Engineering DivisionArgonne National LaboratoryArgonneUSA
  2. 2.Department of Chemistry and PhysicsChicago State UniversityChicagoUSA
  3. 3.Protein Nucleic Acid Interaction Section, Structural Biophysics Laboratory, NCI-Frederick National Institutes of HealthFrederickUSA

Personalised recommendations