Do we live in a quantum world? Advances in multidimensional coherent spectroscopies refine our understanding of quantum coherences and structural dynamics of biological systems

Current Opinion in Structural Biology

Volumn 16, Issue 5, 2006, Pages 654-663

  Nagy, Andrea ^a   Prokhorenko, Valentyn ^a   Miller, RJ Dwayne ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; PROTON PUMP; WATER;

ENERGY TRANSFER; HYDROGEN BOND; INFRARED SPECTROSCOPY; LASER; LIGHT HARVESTING SYSTEM; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; QUANTUM MECHANICS; REVIEW; SPECTROSCOPY; TEMPERATURE DEPENDENCE;

ANIMALS; BIOCHEMISTRY; HUMANS; HYDROGEN BONDING; PHOTOSYNTHESIS; QUANTUM THEORY; RETINALDEHYDE; SPECTROPHOTOMETRY, INFRARED; WATER;

EID: 33749052948     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2006.08.012     Document Type: Review

References (48)

1. Schrödinger E. What is Life?: The Physical Aspects of the Living Cell with Mind and Matter and Autobiographical Sketches (1992), Cambridge University Press, Cambridge
2. Glauber R.J. Quantum theory of optical coherence. Phys Rev 130 (1963) 2529-2539
3. Bardeen C.J., and Shank C.V. Ultrafast dynamics of the solvent-solute interaction measured by femtosecond four-wave mixing: LD690 in n-alcohols. Chem Phys Lett 226 (1994) 310-316
4. Cong P.J., Deuel H.P., Yan Y.J., and Simon J.D. Ultrafast electronic dephasing dynamics of large molecules in room-temperature liquids studied by variable pulse-width tunable femtosecond transient absorption-spectroscopy. J Luminescence 60-61 (1994) 699-702
5. Mukamel S. Multidimensional femtosecond correlation spectroscopies of electronic and vibrational excitations. Annu Rev Phys Chem 51 (2000) 691-729
6. Cardoza D., Langhojer F., Trallero-Herrero C., Monti O.L.A., and Weinacht T. Changing pulse-shape basis for molecular learning control. Phys Rev A 70 (2004) 053406
7. Hamm P., Lim M.H., and Hochstrasser R.M. Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy. J Phys Chem B 102 (1998) 6123-6138
8. Woutersen S., and Hamm P. Nonlinear two-dimensional vibrational spectroscopy of peptides. J Phys Condens Matter 14 (2002) R1035-R1062
9. Zanni M.T., Ge N.H., Kim Y.S., Decatur S.M., and Hochstrasser R.M. The temperature dependent structure distribution of a helical peptide studied with 2D IR spectroscopy. Biophys J 82 (2002) 14A
10. Park J., and Hochstrasser R.M. Multidimensional infrared spectroscopy of a peptide intramolecular hydrogen bond. Chem Phys 323 (2006) 78-86. The power of 2D IR spectroscopy is demonstrated with for an acylproline dipeptide. At least two different intramolecular hydrogen-bonded structures were revealed that are fairly rigid and undergo internal dynamic exchange.
11. 10- and α-helical conformations in early events of protein folding.
12. Smith A.W., Chung H.S., Ganim Z., and Tokmakoff A. Residual native structure in a thermally denatured beta-hairpin. J Phys Chem B 109 (2005) 17025-17027
13. Bredenbeck J., Helbing J., Behrendt R., Renner C., Moroder L., Wachtveitl J., and Hamm P. Transient 2D-IR spectroscopy: snapshots of the nonequilibrium ensemble during the picosecond conformational transition of a small peptide. J Phys Chem B 107 (2003) 8654-8660
14. Chung H.S., Khalil M., and Tokmakoff A. Nonlinear infrared spectroscopy of protein conformational change during thermal unfolding. J Phys Chem B 108 (2004) 15332-15342
15. Hahn S., Kim S.S., Lee C., and Cho M. Characteristic two-dimensional IR spectroscopic features of antiparallel and parallel beta-sheet polypeptides: simulation studies. J Chem Phys 123 (2005) 084905
16. Fang C., Wang J., Charnley A.K., Barber-Armstrong W., Smith A.B., Decatur S.M., and Hochstrasser R.M. Two-dimensional infrared measurements of the coupling between amide modes of an alpha-helix. Chem Phys Lett 382 (2003) 586-592
17. Rubtsov I.V., Kumar K., and Hochstrasser R.M. Dual-frequency 2D IR photon echo of a hydrogen bond. Chem Phys Lett 402 (2005) 439-443. A significant advance in 2D IR to include multiple resonances in analogy to heteronuclear NMR. This work expands upon the first report [18] to determine the coupling between NH and C{double bond, long}O modes in forming hydrogen bonds and the positive correlation of these modes to the bath (modulation of the hydrogen bond strength through solvent fluctuations affects both modes in the same way).
18. Rubtsov I.V., Wang J.P., and Hochstrasser R.M. Dual-frequency 2D-IR spectroscopy heterodyned photon echo of the peptide bond. Proc Natl Acad Sci USA 100 (2003) 5601-5606
19. Hamm P. Three-dimensional-IR spectroscopy: beyond the two-point frequency fluctuation correlation function. J Chem Phys 124 (2006) 124506
20. Zolotarev V.M., Mikhlinov B.A., Alperovich L.I., and Popov S.I. Dispersion and absorption of liquid water in the infrared and radio regions of the spectrum. Opt Spectrosc 27 (1969) 430-432
21. Hale G.M., and Querry M.R. Optical constants of water in the 200 nm to 200 μm wavelength region. Appl Opt 12 (1973) 555-563
22. Eisenberg D., and Kauzmann W. The Structure and Properties of Water (1969), Oxford University Press, New York
23. Stenger J., Madsen D., Dreyer J., Nibbering E.T.J., Hamm P., and Elsaesser T. Coherent response of hydrogen bonds in liquids probed by ultrafast vibrational spectroscopy. J Phys Chem A 105 (2001) 2929-2932
24. Nibbering E.T.J., and Elsaesser T. Ultrafast vibrational dynamics of hydrogen bonds in the condensed phase. Chem Rev 104 (2004) 1887-1914. A comprehensive review of our current understanding of hydrogen-bond dynamics.
25. Asbury J.B., Steinel T., Stromberg C., Corcelli S.A., Lawrence C.P., Skinner J.L., and Fayer M.D. Water dynamics: vibrational echo correlation spectroscopy and comparison to molecular dynamics simulations. J Phys Chem A 108 (2004) 1107-1119. This article gives a good, concise account of experiment and theory for studying hydrogen-bond dynamics.
26. 2O by introducing nanofluidics and diffractive optics to 2D IR. Nanofluidics have potential applications in areas currently using microfluidics.
27. Paarmann A, Kraemer D, Cowan ML, Bruner BD, Miller RJD, Huse N, Dwyer JR, Nibbering ETJ, Elsaesser T: Ultrafast phenomena XV. In Springer Series in Chemical Physics. Edited by Miller RJD, Weiner AM, Corkum P, Jonas DM. Berlin: Springer; 2006:in press.
28. Davydov A.S. Theory of Molecular Excitons (1971), Plenum Press, New York
29. van Amerongen H., Valkunas L., and van Grondelle R. Photosynthetic Excitons. edn 1 (2000), World Scientific Co, Singapore
30. Brixner T., Stenger J., Vaswani H.M., Cho M., Blankenship R.E., and Fleming G.R. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434 (2005) 625-628. The first report of 2D-E spectroscopy of a biological system. This work gives femtosecond time resolution with nanometer spatial resolution for the energy transfer process in the model light-harvesting FMO complex.
31. ••].
32. Louwe R.J.W., Vrieze J., Hoff A.J., and Aartsma T.J. Toward an integral interpretation of the optical steady-state spectra of the FMO-complex of Prosthecochloris aestuarii. 2. Exciton simulations. J Phys Chem B 101 (1997) 11280-11287
33. Cho M.H., and Fleming G.R. The integrated photon echo and solvation dynamics. II. Peak shifts and two-dimensional photon echo of a coupled chromophore system. J Chem Phys 123 (2005) 114506
34. Shapiro M., and Brumer P. Principles of the Quantum Control of Molecular Processes. edn 1 (2002), John Wiley & Sons, Inc, Hoboken
35. Herek J.L., Wohlleben W., Cogdell R.J., Zeidler D., and Motzkus M. Quantum control of energy flow in light harvesting. Nature 417 (2002) 533-535
36. Wohlleben W., Buckup T., Herek J.L., and Motzkus M. Coherent control for spectroscopy and manipulation of biological dynamics. Chemphyschem 6 (2005) 850-857. This paper gives both more experimental details on the study described in [35] and further predictions for testing their proposed mechanism of control. A discussion of future applications of coherent control in biology with respect to studying mode-selective chemistry is given.
37. Prokhorenko V.I., Nagy A.M., and Miller R.J.D. Coherent control of the population transfer in complex solvated molecules at weak excitation. An experimental study. J Chem Phys 122 (2005) 184502. This work was a necessary precursor to the study of biological molecules to show that coherent control under weak field conditions could be employed to ensure the states prepared by the laser excitation pertain to the same levels involved in light activated biological processes.
38. Papagiannakis E., Vengris M., Valkunas L., Cogdell R.J., van Grondelle R., and Larsen D.S. Excited-state dynamics of carotenoids in light-harvesting complexes. 2. Dissecting pulse structures from optimal control experiments. J Phys Chem B 110 (2006) 5737-5746. This paper describes studies of the effects of high excitation energies, typically used in coherent control studies, that lead to new relaxation pathways and intermediates not found under low excitation and need to be taken into account in determining the dynamics under coherent control at high excitation.
39. Hauer J., Buckup T., and Motzkus M. Enhancement of molecular modes by electronically resonant multipulse excitation: further progress towards mode selective chemistry. J Chem Phys 125 (2006) 061101. Open-loop control of β-carotene as a model for biological systems shows selective coherent excitation of Raman active modes in the excited electronic state.
40. Tittor J., and Oesterhelt D. The quantum yield of bacteriorhodopsin. FEBS Lett 263 (1990) 269-273
41. Mathies R.A., Cruz C.H.B., Pollard W.T., and Shank C.V. Direct observation of the femtosecond excited-state cis-trans isomerization in bacteriorhodopsin. Science 240 (1988) 777-779
42. Schoenlein R.W., Peteanu L.A., Mathies R.A., and Shank C.V. The first step in vision - femtosecond isomerization of rhodopsin. Science 254 (1991) 412-415
43. Prokhorenko VI, Nagy AM, Waschuk SA, Brown LS, Birge RR, Miller RJD: Coherent control of retinal isomerization in bacteriorhodopsin. Science 2006, in press. Enhancement and suppression of the functional response of a biological system is reported. The control involves the displacement of heavy atoms, that is, control of the efficiency with which work is done by the biological system in a manner consistent with exploitation of quantum coherence effects.
44. Ogilvie J.P., Cowan M.L., Armstrong M.R., Nagy A.M., and Miller R.J.D. Diffractive optics-based heterodyne detected three-pulse photon echo. In: Miller R.J.D., Murnane M.M., Scherer N.F., and Weiner A.M. (Eds). Springer Series in Chemical Physics 71 (2003), Springer-Verlag, New York 571-573
45. Dadusc G., Goodno G.D., Chiu H.L., Ogilvie J., and Miller R.J.D. Advances in grating-based photoacoustic spectroscopy for the study of protein dynamics. Isr J Chem 38 (1998) 191-206
46. Goodno G.D., Dadusc G., and Miller R.J.D. Ultrafast heterodyne-detected transient-grating spectroscopy using diffractive optics. J Opt Soc Am B 15 (1998) 1791-1794
47. Cowan M.L., Ogilvie J.P., and Miller R.J.D. Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes. Chem Phys Lett 386 (2004) 184-189. This is an extension of the work discussed in [41], which first solved phase stabilization of photon echo spectroscopy using both anti-correlated noise and variable glass delays in the interferometer design for the second independent time delay needed for 2D spectroscopy.
48. Judson R.S., and Rabitz H. Teaching lasers to control molecules. Phys Rev Lett 68 (1992) 1500-1503