Site-specific solvation of the photoexcited protochlorophyllide a in methanol: Formation of the hydrogen-bonded intermediate state induced by hydrogen-bond strengthening

Biophysical Journal

Volumn 94, Issue 1, 2008, Pages 38-46

  Zhao, Guang Jiu ^a   Han, Ke Li ^a  

^a DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

METHANOL; PROTOCHLOROPHYLLIDE;

ARTICLE; BINDING AFFINITY; FLUORESCENCE SPECTROSCOPY; HYDROGEN BOND; PROTEIN BINDING; SOLVATION;

EID: 37749035607     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.113738     Document Type: Article

References (63)

1. Suzuki, J. Y., D. W. Bolivar, and C. E. Bauer. 1997. Genetic analysis of chlorophyll biosynthesis. Annu. Rev. Genet. 31:61-89.
2. Lebedev, N., and M. P. Timko. 1998. Protochlorophyllide photoreduction. Photosynth. Res. 58:5-23.
3. Bollivar, D. W. 2006. Recent advances in chlorophyll biosynthesis. Photosynth. Res. 90:173-194.
4. Cornah, J. E., M. J. Terry, and A. G. Smith. 2003. Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci. 8:224-230.
5. Eckhardt, U., B. Grimm, and S. Hörtensteiner. 2004. Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol. Biol. 56:1-14.
6. Moulin, M., and A. G. Smith. 2005. Regulation of tetrapyrrole biosynthesis in higher plants. Biochem. Soc. Trans. 33:737-742.
7. Schoefs, B., and F. Franck. 2003. Protochlorophyllide reduction: mechanisms and evolution. Photochem. Photobiol. 78:543-557.
8. Masuda, T., and K. Takamiya. 2004. Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms. Photosynth. Res. 81:1-29.
9. Yang, J., and Q. Cheng. 2004. Origin and evolution of the light-dependent protochlorophyllide oxidoreductase (LPOR) genes. Plant Biol. 6:537-544.
10. Heyes, D. J., C. N. Hunter, I. H. M. van Stokkum, and R. van Grondelle. 2003. Ultrafast enzymatic reaction dynamics in protochlorophyllide oxidoreductase. Nat. Struct. Biol. 10:491-492.
11. Deng, H., R. Callender, and E. Howell. 2001. Vibrational structure of dihydrofolate bound to R67 dihydrofolate reductase. J. Biol. Chem. 276:48956-48960.
12. Cheng, H., I. Nikolic-Hughes, J. H. H. Wang, H. Deng, P. J. O'Brien, L. Wu, Z. Y. Zhang, D. Herschlag, and R. Callender. 2002. Environmental effects on phosphoryl group bonding probed by vibrational spectroscopy: implications for understanding phosphoryl transfer and enzymatic catalysis. J. Am. Chem. Soc. 124:11295-11306.
13. McClendon, S., N. Zhadin, and R. Callender. 2005. The approach to the Michaelis complex in lactate dehydrogenase: the substrate binding pathway. Biophys. J. 89:2024-2032.
14. Callender, R., and R. B. Dyer. 2006. Advances in time-resolved approaches to characterize the dynamical nature of enzymatic catalysis. Chem. Rev. 106:3031-3042.
15. Zuo, P., B. X. Li, X. H. Zhao, Y. S. Wu, X. C. Ai, J. P. Zhang, L. B. Li, and T. Y. Kuang. 2006. Ultrafast carotenoid-to-chlorophyll singlet energy transfer in the cytochrome b(6)f complex from Bryopsis corticulans. Biophys. J. 90:4145-4154.
16. Wang, Y. L., and X. C. Hu. 2002. Quantum chemistry study of π-π stacking interactions of the bacteriochlorophyll dimer in the photosynthetic reaction center of Rhodobacter sphaeroides. J. Chem. Phys. 117:1-4.
17. Wang, Y. L., and X. C. Hu. 2002. A quantum chemistry study of binding carotenoids in the bacterial light-harvesting complexes. J. Am. Chem. Soc. 124:8445-8451.
18. Mao, L. S., Y. L. Wang, and X. C. Hu. 2003. π-π stacking interactions in the peridinin-chlorophyll-protein of Amphidinium carterae. J. Phys. Chem. B. 107:3963-3971.
19. Wang, Y. L., L. S. Mao, and X. C. Hu. 2004. Insight into the structural role of carotenoids in the Photosystem I: a quantum chemical analysis. Biophys. J. 86:3097-3111.
20. Zhang, D. W., and J. Z. H. Zhang. 2004. Full ab initio computation of protein-water interaction energies. J. Theor. Comput. Chem. 3:43-49.
21. Mei, Y., E. L. Wu, K. L. Han, and J. Z. H. Zhang. 2006. Treating hydrogen bonding in ab initio calculation of biopolymers. Int. J. Quantum Chem. 106:1267-1276.
22. Mei, Y., C. G. Ji, and J. Z. H. Zhang. 2006. A new quantum method for electrostatic solvation energy of protein. J. Chem. Phys. 125:094906.
23. York, D. M., T. S. Lee, and W. T. Yang. 1996. Quantum mechanical study of aqueous polarization effects on biological macromolecules. J. Am. Chem. Soc. 118:10940-10941.
24. York, D. M., T. S. Lee, and W. T. Yang. 1998. Quantum mechanical treatment of biological macromolecules in solution using linear-scaling electronic structure methods. Phys. Rev. Lett. 80:5011-5014.
25. Hori, T., H. Takahashi, M. Nakano, T. Nitta, and W. T. Yang. 2006. A QM/MM study combined with the theory of energy representation: solvation free energies for anti/syn acetic acids in aqueous solution. Chem. Phys. Lett. 419:240-244.
26. Karmacharya, R., D. Antoniou, and S. D. Schwartz. 2001. Nonequilibrium solvation and the quantum Kramers problem: proton transfer in aqueous glycine. J. Phys. Chem. A. 105:2563-2567.
27. Nunez, S., D. Antoniou, V. L. Schramm, and S. D. Schwartz. 2004. Promoting vibrations in human purine nucleoside phosphorylase. A molecular dynamics and hybrid quantum mechanical/molecular mechanical study. J. Am. Chem. Soc. 126:15720-15729.
28. Basner, J. E., and S. D. Schwartz. 2005. How enzyme dynamics helps catalyze a reaction in atomic detail: a transition path sampling study. J. Am. Chem. Soc. 127:13822-13831.
29. Antoniou, D., J. Basner, S. Nunez, and S. D. Schwartz. 2006. Computational and theoretical methods to explore the relation between enzyme dynamics and catalysis. Chem. Rev. 106:3170-3187.
30. Exequiel, J. R., T. Pineda, R. Callender, and S. D. Schwartz. 2007. Ligand binding and protein dynamics in lactate dehydrogenase. Biophys. J. 10.1529/biophysj.107.106146.
31. Dietzek, B., R. Maksimenka, T. Siebert, E. Birckner, W. Kiefer, J. Popp, G. Hermann, and M. Schmitt. 2004. Excited-state processes in protochlorophyllide a: a femtosecond time-resolved absorption study. Chem. Phys. Lett. 397:110-115.
32. Dietzek, B., W. Kiefer, J. Popp, G. Hermann, and M. Schmitt. 2006. Solvent effects on the excited-state processes of protochlorophyllide: a femtosecond time-resolved absorption study. J. Phys. Chem. B. 110:4399-4406.
33. Dietzek, B., W. Kiefer, A. Yartsev, V. Sundström, P. Schellenberg, P. Grigaravicius, G. Hermann, J. Popp, and M. Schmitt. 2006. The excited-state chemistry of protochlorophyllide a: a time-resolved fluorescence study. ChemPhysChem. 7:1727-1733.
34. El Hamouri, B., M. Brouers, and C. Sironval. 1981. Pathway from photoinactive P633-628 protochlorophyllide to the P696-682 chlorophyllide in cucumber etioplast suspensions. Plant Sci. Lett. 21:375-379.
35. Ryderg, M., and C. Sundqvist. 1982. Spectral forms of protochlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol. Plant. 56:133-138.
36. Böddi, B., A. Lindsten, M. Ryderg, and C. Sundqvist. 1989. On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol. Plant. 76:135-143.
37. + and protochlorophyllide-NADPH complexes and their regeneration after flash illumination in leaves and etioplast membranes of dark-grown wheat. Photosynth. Res. 59:53-61.
38. Mysliwa-Kurdziel, B., F. Franck, and K. Strzalka. 1999. Analysis of fluorescence lifetime of protochlorophyllide and chlorophyllide in isolated etioplast membranes measured from multifrequency cross-correlation phase fluorometry. Photochem. Photobiol. 70:616-623.
39. Shipman, L. I., T. M. Cotton, J. R. Norris, and J. J. Katz. 1976. An analysis of the visible absorption spectrum of chlorophyll a monomer, dimer, and oligomers in solution. J. Am. Chem. Soc. 98:8222-8230.
40. Renge, I., and R. Avarmaa. 1985. Specific solvation of chlorophyll a: solvent nucleophility, hydrogen bonding and steric effects on absorption spectra. Photochem. Photobiol. 42:253-260.
41. Krawczyk, S. 1989. The effects of hydrogen bonding and coordination interaction in visible absorption and vibrational spectra of chlorophyll a. Biochim. Biophys. Acta. 976:140-149.
42. y energies of bacterio-chlorophyll a and bacteriopheophytin a. Photochem. Photobiol. 65:330-337.
43. Vladkova, R. 2000. Chlorophyll a self-assembly in polar solvent-water mixtures. Photochem. Photobiol. 71:71-83.
44. Mysliwa-Kurdziel, B., J. Kruk, and K. Strzalka. 2004. Fluorescence lifetimes and spectral properties of protochlorophyllide in organic solvents in relation to the respective parameters in vivo. Photochem. Photobiol. 79:62-67.
45. Sobolewski, A. L., and W. Domcke. 1999. Photophysics of malonaldehyde: an ab initio study. J. Phys. Chem. A. 103:4494-4504.
46. Sobolewski, A. L., and W. Domcke. 1999. Ab initio investigations on the photophysics of indole. Chem. Phys. Lett. 315:293-298.
47. Sobolewski, A. L., and W. Domcke. 2000. Photoejection of electrons from pyrrole into an aqueous environment: ab initio results on pyrrole-water clusters. Chem. Phys. Lett. 321:479-484.
48. Sudholt, W., A. Staib, A. L. Sobolewski, and W. Domcke. 2000. Molecular-dynamics simulations of solvent effects in the intramolecular charge transfer of 4-(N,N-dimethylamino)benzonitrile. Phys. Chem. Chem. Phys. 2:4341-4353.
49. Sobolewski, A. L., and W. Domcke. 2004. Intramolecular hydrogen bonding in the S1(π-π*) excited state of anthranilic acid and salicylic acid: TDDFT calculation of excited-state geometries and infrared spectra. J. Phys. Chem. A. 108:10917-10922.
50. Sobolewski, A. L., W. Domcke, and C. Hattig. 2006. Photophysics of organic photostabilizers. Ab initio study of the excited-state deactivation mechanisms of 2-(2′-hydroxyphenyl)benzotriazole. J. Phys. Chem. A. 110:6301-6306.
51. Zhao, G.-J., and K.-L. Han. 2007. Early time hydrogen-bonding dynamics of photoexcited coumarin 102 in hydrogen-donating solvents: theoretical study. J. Phys. Chem. A. 111:2469-2474.
52. Zhao, G.-J., and K.-L. Han. 2007. Ultrafast hydrogen bond strengthening of the photoexcited fluorenone in alcohols for facilitating the fluorescence quenching. J. Phys. Chem. A. 10.1021/jp0719659.
53. Zhao, G.-J., J.-Y. Liu, L.-C. Zhou, and K.-L. Han. 2007. Site-selective photoinduced electron transfer from alcoholic solvents to the chromophore facilitated by hydrogen bonding: a new fluorescence quenching mechanism. J. Phys. Chem. B. 111:8940-8945.
54. Zhao, G.-J., and K.-L. Han. 2007. Novel infrared spectra for intermolecular dihydrogen bonding of the phenol-borane-trimethylamine complex in electronically excited state. J. Chem. Phys. 127:024306.
55. Furche, F., and R. Ahlrichs. 2002. Adiabatic time-dependent density functional methods for excited state properties. J. Chem. Phys. 117:7433-7447.
56. Whitten, J. L. 1973. Coulombic potential energy integrals and approximations. J. Chem. Phys. 58:4496-4501.
57. Dunlap, B. I., J. W. D. Conolly, and J. R. Sabin. 1979. On some approximations in applications of Xα theory. J. Chem. Phys. 71:3396-3402.
58. Vahtras, O., J. E. Almlöf, and M. W. Feyereisen. 1993. Integral approximations for LCAO-SCF calculations. Chem. Phys. Lett. 213:514-518.
59. Schäfer, A., C. Huber, and R. Ahlrichs. 1994. Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr. J. Chem. Phys. 100:5829-5835.
60. Ahlrichs, R., M. Bär, H. Horn, and C. Kölmel. 1989. Electronic structure calculations on workstation computers: the program system turbomole. Chem. Phys. Lett. 162:165-169.
61. Neugebauer, J., and M. Reiher. 2004. Vibrational center-ligand coupling in transition metal complexes. J. Comput. Chem. 25:587-597.
62. Weigend, F. 2002. A fully direct RI-HF algorithm: implementation, optimised auxiliary basis sets, demonstration of accuracy and efficiency. Phys. Chem. Chem. Phys. 4:4285-4291.
63. Jacquemin, D., E. A. Perpète, G. Scalmani, M. J. Frisch, X. Assfeld, I. Ciofini, and C. Adamo. 2006. Time-dependent density functional theory investigation of the absorption, fluorescence, and phosphorescence spectra of solvated coumarins. J. Chem. Phys. 125:164324.