Abstract
Opsins are a broad class of photoactive proteins, found in all classes of living beings from bacteria to higher animals, which work either as light-driven ion pumps or as visual pigments. The photoactive function in opsins is triggered by the ultrafast isomerization of the retinal chromophore around a specific carbon double bond, leading to a highly distorted, spectrally red-shifted photoproduct. Understanding, by either experimental or computational methods, the time course of this photoisomerization process is of utmost importance, both for its biological significance and because opsin proteins are the blueprint for molecular photoswitches. This paper focuses on the ultrafast 11-cis to all-trans isomerization in visual rhodopsins, and has a twofold goal: (i) to review the most recent experimental and computational efforts aimed at exposing the very early phases of photoconversion; and (ii) discuss future advanced experiments and calculations that will allow an even deeper understanding of the process. We present high time resolution pump-probe data, enabling us to follow the wavepacket motion through the conical intersection connecting excited and ground states, as well as femtosecond stimulated Raman scattering data allowing us to track the subsequent structural evolution until the first stable all-trans photoproduct is reached. We conclude by introducing computational results for two-dimensional electronic spectroscopy, which has the potential to provide even greater detail on the evolution of the electronic structure of retinal during the photoisomerization process.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
O. P. Ernst, D. T. Lodowski, M. Elstner, P. Hegemann, L. S. Brown, H. Kandori, Chem. Rev. 2014 114 126.
J. L. Spudich, C. S. Yang, K. H. Jung, E. N. Spudich, Annu. Rev. Cell Dev. Biol. 2000 16 365.
D. Oesterhelt, W. Stoeckenius, Nat. New Biol. 1971 233 149.
W. Stoeckenius, Trends Biochem. Sci. 1985 10 483.
O. A. Sineshchekov, K.-H. Jung, J. L. Spudich, Proc. Natl. Acad. Sci. U. S. A. 2002 99 8989.
F. Zhang, J. Vierock, O. Yizhar, L. E. Fenno, S. Tsunoda, A. Kianianmomeni, M. Prigge, A. Berndt, J. Cushman, J. Polle, J. Magnuson, P. Hegemann, K. Deisseroth, Cell 2011 147 1446.
A. Terakita, Genome Biol. 2005 6 213.
M. B. Nielsen, Chem. Soc. Rev. 2009 38 913.
D. Baylor, Proc. Natl. Acad. Sci. U. S. A. 1996 93 560.
A. Wand, I. Gdor, J. Zhu, M. Sheves, S. Ruhman, Annu. Rev. Phys. Chem. 2013 64 437.
T. Yoshizawa, G. Wald, Nature 1963 197 1279.
R. W. Schoenlein, L. A. Peteanu, R. A. Mathies, C. V. Shank, Science 1991 254 412.
R. A. Mathies, C. H. B. Cruz, W. T. Pollard, C. V. Shank, Science 1988 240 777.
R. Govindjee, S. P. Balshov, T. G. Ebrey, Biophys. J. 1990 58 597.
J. E. Kim, M. J. Tauber, R. A. Mathies, Biochemistry 2001 40 13774.
H. Kandori, Y. Katsuta, M. Ito, H. Sasabe, J. Am. Chem. Soc. 1995 117 2669.
S. L. Logunov, L. Song, M. A. ElSayed, J. Phys. Chem. 1996 100 18586.
P. Hamm, M. Zurek, T. Roschinger, H. Patzelt, D. Oesterhelt, W. Zinth, Chem. Phys. Lett. 1996 263 613.
R. S. Becker, K. Freedman, J. Am. Chem. Soc. 1985 107 1477.
R. R. Birge, Annu. Rev. Phys. Chem. 1990 41 683.
F. Lumento, V. Zanirato, S. Fusi, E. Busi, L. Latterini, F. Elisei, A. Sinicropi, T. Andruniow, N. Ferre, R. Basosi, M. Olivucci, Angew. Chem., Int. Ed. 2007 46 414.
A. Sinicropi, E. Martin, M. Ryazantsev, J. Helbing, J. Briand, D. Sharma, J. Léonard, S. Haacke, A. Cannizzo, M. Chergui, V. Zanirato, S. Fusi, F. Santoro, R. Basosi, N. Ferré, M. Olivucci, Proc. Natl. Acad. Sci. U. S. A. 2008 105 17642.
D. J. Tannor, Introduction to Quantum Mechanics: A Time Dependent Perspective, University Science Press, Sausalito, 2007.
M. Garavelli, P. Celani, F. Bernardi, M. A. Robb, M. Olivucci, J. Am. Chem. Soc. 1997 119 6891.
R. Gonzalez-Luque, M. Garavelli, F. Bernardi, M. Merchan, M. A. Robb, M. Olivucci, Proc. Natl. Acad. Sci. U. S. A. 2000 97 9379.
M. Klessinger, and J. Michl, Excited States and Photochemistry of Organic Molecules, VCH Publishers, New York, 1994.
B. G. Levine, T. M. Martinez, Annu. Rev. Phys. Chem. 2007 58 613.
T. J. Martinez, Nature 2010 467 412.
F. Gai, K. C. Hasson, P. A. Anfinrud, Proc. Natl. Acad. Sci. U. S. A. 1996 93 15124.
F. Gai, K. C. Hasson, J. C. McDonald, P. A. Anfinrud, Science 1998 279 1886.
T. Kobayashi, T. Saito, H. Otani, Nature 2001 414 531.
S. Ruhman, B. X. Hou, N. Friedman, M. Ottolenghi, M. Sheves, J. Am. Chem. Soc. 2002 124 8854.
M. Olivucci, A. Lami, F. Santoro, Angew. Chem., Int. Ed. 2005 44 5118.
A. Kahan, O. Nahmias, N. Friedman, M. Sheves, S. Ruhman, J. Am. Chem. Soc. 2007 129 537.
B. Loevsky, A. Wand, O. Bismuth, N. Friedman, M. Sheves, S. Ruhman, J. Am. Chem. Soc. 2011 133 1626.
J. B. Hurley, T. G. Ebrey, B. Honig, M. Ottolenghi, Nature 1977 270 540.
R. R. Birge, Biochim. Biophys. Acta 1990 1016 293.
L. Song, M. El-Sayed, J. Am. Chem. Soc. 1998 120 8889.
J. Herbst, K. Heyne, R. Diller, Science 2002 297 822.
A. Warshel, Z. T. Chu, J. Phys. Chem. B 2001 105 9587.
A. Cembran, F. Bernardi, M. Olivucci, M. Garavelli, Proc. Natl. Acad. Sci. U. S. A. 2005 102 6255.
S. A. Kovalenko, A. L. Dobryakov, J. Ruthmann, N. P. Ernsting, Phys. Rev. A 1999 59 2369.
Z. Vardeny, J. Tauc, Opt. Commun. 1981 39 396.
D. Polli, D. Brida, S. Mukamel, G. Lanzani, G. Cerullo, Phys. Rev. A 2010 82 053809.
G. Cerullo, S. de Silvestri, Rev. Sci. Instrum. 2003 74 1.
D. Brida, C. Manzoni, G. Cirmi, M. Marangoni, S. Bonora, P. Villoresi, S. de Silvestri, G. Cerullo, J. Opt. 2010 12 013001.
C. Manzoni, D. Polli, G. Cerullo, Rev. Sci. Instrum. 2006 77 023103.
D. Polli, L. Lüer, G. Cerullo, Rev. Sci. Instrum. 2007 78 103108.
M. Bargheer, N. Zhavoronkov, M. Woerner, T. Elsaesser, ChemPhysChem 2006 7 783.
M. Gao, C. Lu, H. Jean-Ruel, L. C. Liu, A. Marx, K. Onda, S. Koshihara, Y. Nakano, X. Shao, T. Hiramatsu, G. Saito, H. Yamochi, R. R. Cooney, G. Moriena, G. Sciaini, R. J. Dwayne Miller, Nature 2013 496 343.
D. W. McCamant, P. Kukura, R. A. Mathies, J. Phys. Chem. A 2003 107 8208.
D. W. McCamant, P. Kukura, S. Yoon, R. A. Mathies, Rev. Sci. Instrum. 2004 75 4971.
P. Kukura, D. W. McCamant, R. A. Mathies, Annu. Rev. Phys. Chem. 2007 58 461.
C. Fang, R. R. Frontiera, R. Tran, R. A. Mathies, Nature 2009 462 200.
T. Brixner, J. Stenger, H. M. Vaswani, M. Cho, R. E. Blankenship, G. R. Fleming, Nature 2005 434 625.
E. Collini, C. Y. Wong, K. E. Wilk, P. M. G. Curmi, P. Brumer, G. D. Scholes, Nature 2010 463 644.
S. Mukamel, Annu. Rev. Phys. Chem. 2000 51 691.
P. Hamm, and M. Zanni, Concepts and Methods of 2D Infrared Spectroscopy, Cambridge University Press, 2011.
M. L. Cowan, J. P. Ogilvie, R. J. D. Miller, Chem. Phys. Lett. 2004 386 184.
T. Brixner, I. V. Stiopkin, G. R. Fleming, Opt. Lett. 2004 29 884.
S. H. Shim, D. B. Strasfeld, Y. L. Ling, M. T. Zanni, Proc. Natl. Acad. Sci. U. S. A. 2007 104 14197.
E. M. Grumstrup, S. H. Shim, M. A. Montgomery, N. H. Damrauer, M. T. Zanni, Opt. Express 2007 15 16681.
P. F. Tekavec, J. A. Myers, K. L. M. Lewis, J. P. Ogilvie, Opt. Lett. 2009 34 1390.
D. Brida, C. Manzoni, G. Cerullo, Opt. Lett. 2012 37 3027.
Computational Photochemistry, ed. M. Olivucci, Elsevier, Amsterdam, 2005, vol. 16.
K. Andersson, P.-A. Malmqvist, B. O. Roos, J. Chem. Phys. 1992 96 1218.
I. Rivalta, A. Nenov, G. Cerullo, S. Mukamel, M. Garavelli, Int. J. Quantum Chem. 2014 114 85.
A. Nenov, I. Rivalta, G. Cerullo, S. Mukamel, M. Garavelli, J. Phys. Chem. Lett. 2014 5 767.
P. Altoè, M. Stenta, A. Bottoni, M. Garavelli, Theor. Chem. Acc. 2007 118 219.
G. Groenhof, et al. Adv. Quantum Chem. 2010 59 181.
M. Barbatti, Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2011 1 620.
H. M. Senn, W. Thiel, Top. Curr. Chem. 2007 268 173.
P. Cieplak, F.-Y. Dupradeau, Y. Duan, J. Wang, J. Phys.: Condens. Mater 2009 21 333102.
W. Chen, W. L. Hase, B. Schlegel, Chem. Phys. Lett. 1994 228 436.
B. H. Lengsfield, D. R. Yarkony, Adv. Chem. Phys. 1992 82 1.
J. Stalring, B. Anders, R. Lindh, Mol. Phys. 2001 99 103.
L. Verlet, Phys. Rev. 1967 159 98.
J. C. Tully, J. Chem. Phys. 1990 93 1061.
J. C. Tully, Int. J. Quant. Chem., Quantum Biol. Symp. 1991 40 299.
E. Fabiano, T. W. Keal, W. Thiel, Chem. Phys. 2008 349 334.
G. Granucci, M. Persico, J. Chem. Phys. 2007 126 134114.
W. J. DeGrip, F. J. M. Daemen, S. L. Bonting, Methods Enzymol. 1980 67 301.
D. Polli, P. Altoe, O. Weingart, K. M. Spillane, C. Manzoni, D. Brida, G. Tomasello, G. Orlandi, P. Kukura, R. A. Mathies, M. Garavelli, G. Cerullo, Nature 2010 467 440.
L. A. Peteanu, R. W. Schoenlein, Q. Wang, R. A. Mathies, C. V. Shank, Proc. Natl. Acad. Sci. U. S. A. 1993 90 11762.
Q. Wang, R. W. Schoenlein, L. A. Peteanu, R. A. Mathies, C. V. Shank, Science 1994 266 422.
P. Kukura, D. W. McCamant, S. Yoon, D. B. Wandschneider, R. A. Mathies, Science 2005 310 1006.
A. Warshel, Nature 1976 260 679.
A. Warshel, N. Barboy, J. Am. Chem. Soc. 1982 104 1469.
T. Okada, M. Sugihara, A. N. Bondar, M. Elstner, P. Entel, V. Buss, J. Mol. Biol. 2004 342 571.
R. W. Schoenlein, L. A. Peteanu, Q. Wang, R. A. Mathies, C. V. Shank, J. Phys. Chem. 1993 97 12087.
J. Fan, B. Rohrer, G. Moiseyev, J. Ma, R. K. Crouch, Proc. Natl. Acad. Sci. U. S. A. 2003 100 13662.
T. Yoshizawa, G. Wald, Nature 1963 197 1279.
S. J. Hug, J. W. Lewis, D. S. Kliger, J. Am. Chem. Soc. 1988 110 1998.
D. Polli, O. Weingart, D. Brida, E. Poli, M. Maiuri, K. M. Spillane, A. Bottoni, P. Kukura, R. A. Mathies, G. Cerullo, M. Garavelli, Angew. Chem., Int. Ed. 2014 53 2504.
W. C. Chung, S. Nanbu, T. Ishida, J. Phys. Chem. B 2012 116 8009.
A. Strambi, P. B. Coto, L. M. Frutos, N. Ferré, M. Olivucci, J. Am. Chem. Soc. 2008 130 3382.
J. D. Biggs, S. Mukamel, J. Chem. Phys. 2011 134 161101.
E. C. Y. Yan, Z. Ganim, M. A. Kazmi, B. S. W. Chang, T. P. Sakmar, R. A. Mathies, Biochemistry 2004 43 10867.
I. Rivalta, A. Nenov, O. Weingart, G. Cerullo, M. Garavelli, S. Mukamel, J. Phys. Chem. B 2014 118 8396.
G. Zgrablic, K. Voitchovsky, M. Kindermann, S. Haacke, M. Chergui, Biophys. J. 2005 88 2779.
I. Rivalta, A. Nenov, M. Garavelli, Phys. Chem. Chem. Phys. 2014 16 16865.
V. I. Prokhorenko, A. M. Nagy, S. A. Waschuk, L. S. Brown, R. R. Birge, R. J. D. Miller, Science 2006 313 1257.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Polli, D., Rivalta, I., Nenov, A. et al. Tracking the primary photoconversion events in rhodopsins by ultrafast optical spectroscopy. Photochem Photobiol Sci 14, 213–228 (2015). https://doi.org/10.1039/c4pp00370e
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c4pp00370e