Journal of Molecular Modeling

, Volume 19, Issue 6, pp 2329–2334 | Cite as

Comparative studies for evaluation of CO2 fixation in the cavity of the Rubisco enzyme using QM, QM/MM and linear-scaling DFT methods

Original Paper

Abstract

We evaluate the minimum energy configuration (MM) and binding free energy (QM/MM and QM) of CO2 to Rubisco, of fundamental importance to the carboxylation step of the reaction. Two structural motifs have been used to achieve this goal, one of which starts from the initial X-ray Protein Data Bank structure of Rubisco’s active centre (671 atoms), and the other is a simplified, smaller model (77 atoms) which has been used most successfully, thus far, for study. The small model is subjected to quantum chemical density functional theory (DFT) studies, both in vacuo and using implicit solvation. The effects of the protein environment are also included by means of a hybrid quantum mechanical/molecular mechanical (QM/MM) approach, using PM6/AMBER and B3LYP/AMBER schemes. Finally, linear-scaling DFT methods have also been applied to evaluate energetic features of the large motif, and the result obtained for the binding free energy of the CO2 underlines the importance of the accurate modelling of the surrounding protein milieu using a full DFT description.

Figure

77 atom representation of the Rubisco active site used in QM calculations

Keywords

Carboxylation step Linear-scaling DFT PM6 QM/MM Rubisco 

References

  1. 1.
    Berg JM, Tymoczko JL, Stryer L (2007) Biochemistry, 6th edn. W. H. Freeman, New YorkGoogle Scholar
  2. 2.
    Griffiths H (2006) Nature 441:940–941CrossRefGoogle Scholar
  3. 3.
    Portis AR, Parry MAJ (2007) Photosynth Res 94:121–143CrossRefGoogle Scholar
  4. 4.
    Spreitzer RJ, Salvucci ME (2002) Annu Rev Plant Biol 53:449–475CrossRefGoogle Scholar
  5. 5.
    Sage RF, Way DA, Kubien DS (2008) J Exp Bot 59:1581–1595CrossRefGoogle Scholar
  6. 6.
    Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ (2003) J Exp Bot 54:1321–1333CrossRefGoogle Scholar
  7. 7.
    Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer, SunderlandGoogle Scholar
  8. 8.
    Galmés J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Plant Cell Environ 28:571CrossRefGoogle Scholar
  9. 9.
    Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) J Exp Bot 60:2235–2248CrossRefGoogle Scholar
  10. 10.
    Mott KA, Woodrow IE (2000) J Exp Bot 51:399–406CrossRefGoogle Scholar
  11. 11.
    Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, Frederick WJ, Hallett JP, Leak DJ, Liotta CL, Mielenz JR, Murphy R, Templer R, Tschaplinski T (2006) Science 311:484CrossRefGoogle Scholar
  12. 12.
    Sage RF, Kubien DS (2007) Plant Cell Environ 30:1086CrossRefGoogle Scholar
  13. 13.
    Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) J Exp Bot 60:2235CrossRefGoogle Scholar
  14. 14.
    Mott KA, Woodrow IE (2000) J Exp Bot 51:399CrossRefGoogle Scholar
  15. 15.
    Kannappan B, Gready JE (2008) J Am Chem Soc 130:15063CrossRefGoogle Scholar
  16. 16.
    King WA, Gready JE, Andrews TJ (1998) Biochemistry-Us 37:15414CrossRefGoogle Scholar
  17. 17.
    Skylaris CK, Haynes PD, Mostofi AA, Payne MC (2005) J Chem Phys 122Google Scholar
  18. 18.
    Hine NDM, Haynes PD, Mostofi AA, Skylaris CK, Payne MC (2009) Comput Phys Commun 180:1041CrossRefGoogle Scholar
  19. 19.
    Gordon MS, Fedorov DG, Pruitt SR, Slipchenko LV (2012) Chem Rev 112:632CrossRefGoogle Scholar
  20. 20.
    Cole DJ, Rajendra E, Roberts-Thomson M, Hardwick B, McKenzie GJ, Payne MC, Venkitaraman AR, Skylaris CK (2011) PLoS Comput Biol. doi:10.1371/journal.pcbi.1002096
  21. 21.
    Cole DJ, Skylaris CK, Rajendra E, Venkitaraman AR, Payne MC (2010) EPL. doi:10.1209/0295-5075/91/37004
  22. 22.
    Bernstein FC, Koetzle TF, Williams GJB, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) Eur J Biochem 80:319CrossRefGoogle Scholar
  23. 23.
    Andersson I (1996) J Mol Biol 259:160–174CrossRefGoogle Scholar
  24. 24.
    Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A (2000) Annu Rev Biophys Biomol 29:291–325CrossRefGoogle Scholar
  25. 25.
    Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA (1995) J Am Chem Soc 117:5179CrossRefGoogle Scholar
  26. 26.
    Wang J, Cieplak P, Kollman PAJ (2000) Comput Chem 21:1049CrossRefGoogle Scholar
  27. 27.
    Aaqvist J (1990) J Phys Chem 94:8021CrossRefGoogle Scholar
  28. 28.
    Harris JG, Yung KH (1995) J Phys Chem 99:12021CrossRefGoogle Scholar
  29. 29.
    Velanga S, Vedam V, Anderson BJ (2011) In 7th International Conference on Gas Hydrates (ICGH 2011), Proc: Edinburgh, Scotland, United Kingdom, 2011Google Scholar
  30. 30.
    Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein MLJ (1983) Chem Phys 79:926Google Scholar
  31. 31.
    Pang YP (2001) Proteins 45:183–189CrossRefGoogle Scholar
  32. 32.
    King WA, Gready JE, Andrews TJ (1998) Biochemistry-Us 37:15414–15422CrossRefGoogle Scholar
  33. 33.
    Oliva M, Safont VS, Andres J, Tapia O (1999) J Phys Chem A 103:8725CrossRefGoogle Scholar
  34. 34.
    Oliva M, Safont VS, Andres J, Tapia O (1999) J Phys Chem A 103:6009CrossRefGoogle Scholar
  35. 35.
    Oliva M, Safont VS, Andres J, Tapia O (2001) Chem Phys Lett 340:391CrossRefGoogle Scholar
  36. 36.
    Tapia O, Andres J, Safont VS (1995) J Mol Struct THEOCHEM 342:131–140CrossRefGoogle Scholar
  37. 37.
    Zhang X, Bruice TC (2007) Biochemistry-Us 46:14838–14844CrossRefGoogle Scholar
  38. 38.
    Becke AD (1993) J Chem Phys 98:5648–5652CrossRefGoogle Scholar
  39. 39.
    Lee CT, Yang WT, Parr RG (1988) Phys Rev B 37:785–789CrossRefGoogle Scholar
  40. 40.
    Gaussian 09, Revision A.1, Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery Jr. JA, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian, Inc., Wallingford CTGoogle Scholar
  41. 41.
    Dapprich S, Komaromi I, Byun KS, Morokuma K, Frisch MJ (1999) J Mol Struct (THEOCHEM) 461:1CrossRefGoogle Scholar
  42. 42.
    Vreven T, Morokuma K, Farkas O, Schlegel HB, Frisch MJ (2003) J Comput Chem 24:760–769CrossRefGoogle Scholar
  43. 43.
    Stewart JJP (2007) J Mol Model 13:1173–1213CrossRefGoogle Scholar
  44. 44.
    Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ (1994) J Phys Chem-Us 98:11623–11627CrossRefGoogle Scholar
  45. 45.
    Tomasi J, Mennucci B, Cammi R (2005) Chem Rev 105:2999–3093CrossRefGoogle Scholar
  46. 46.
    Perdew JP, Burke K, Ernzerhof M (1996) Phys Rev Lett 77:3865–3868CrossRefGoogle Scholar
  47. 47.
    Perdew JP, Wang Y (1992) Phys Rev B 45:13244–13249CrossRefGoogle Scholar
  48. 48.
    Mostofi AA, Haynes PD, Skylaris CK, Payne MC (2003) J Chem Phys 119:8842–8848CrossRefGoogle Scholar
  49. 49.
    Hill Q, Skylaris CK (2009) Public Relat Soc Am 465:669–683Google Scholar
  50. 50.
    Fox S, Wallnoefer HG, Fox T, Tautermann CS, Skylaris CK (2011) J Chem Theory Comput 7:1102–1108CrossRefGoogle Scholar
  51. 51.
    Hine NDM, Robinson M, Haynes PD, Skylaris CK, Payne MC, Mostofi AA (2011) Phys Rev B 83Google Scholar
  52. 52.
    Dziedzic J, Helal HH, Skylaris CK, Mostofi AA, Payne MC (2011) Epl-Europhys Lett 95Google Scholar
  53. 53.
    Murata K, Fedorov DG, Nakanishi I, Kitaura K (2009) J Phys Chem B 113:809CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.The SFI Strategic Research Cluster in Solar Energy ConversionUniversity College DublinDublin 4Ireland
  2. 2.The Centre for Synthesis and Chemical Biology, School of Chemical and Bioprocess EngineeringUniversity College DublinDublin 4Ireland

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