Ultrafast spectroscopy of biological photoreceptors

Current Opinion in Structural Biology

Volumn 17, Issue 5, 2007, Pages 623-630

  Kennis, John TM ^a   Groot, Marie Louise ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; QUERCETIN; RHODOPSIN;

ABSORPTION SPECTROSCOPY; CHROMATOPHORE; DYNAMICS; ELECTRON TRANSPORT; HYDROGEN BOND; INFRARED SPECTROSCOPY; ISOMERIZATION; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTON TRANSPORT; RAMAN SPECTROMETRY; REVIEW; SPECTROSCOPY;

BACTERIAL PROTEINS; FLAVIN-ADENINE DINUCLEOTIDE; HYDROGEN BONDING; MODELS, MOLECULAR; PHOTORECEPTORS, MICROBIAL; PHYTOCHROME; PROTEIN STRUCTURE, TERTIARY; RHODOBACTER SPHAEROIDES; RHODOPSIN; SPECTROPHOTOMETRY; SPECTROPHOTOMETRY, INFRARED; SPECTRUM ANALYSIS, RAMAN; SYNECHOCYSTIS;

EID: 35548998652     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.09.006     Document Type: Review

References (46)

1. Beja O., Spudich E.N., Spudich J.L., Leclerc M., and DeLong E.F. Proteorhodopsin phototrophy in the ocean. Nature 411 (2001) 786-789
2. Christie J.M., and Briggs W.R. In: Briggs W.R., and Spudich J.L. (Eds). Handbook of Photosensory Receptors (2005), Wiley-VCH Verlag GmbH & Co, Weinheim 277-304
3. Losi A. The bacterial counterparts of plant phototropins. Photochem Photobiol Sci 3 (2004) 566-574
4. Crosson S. In: Briggs W.R., and Spudich J.L. (Eds). Handbook of Photosensory Receptors (2005), Wiley-VCH Verlag GmbH & Co, Weinheim 323-336
5. Gomelsky M., and Klug G. BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem Sci 27 (2002) 497-500
6. van der Horst M.A., and Hellingwerf K.J. Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37 (2004) 13-20
7. Lee I.R., Lee W., and Zewail A.H. Primary steps of the photoactive yellow protein: isolated chromophore dynamics and protein directed function. Proc Natl Acad Sci U S A 103 (2006) 258-262. The isomerization of the PYP chromophore (p-coumaric acid, pCA) in molecular beams was investigated by means of femtosecond mass selection and electron detachment techniques. Isomerization was found to proceed at rates and efficiencies similar to that of pCA bound to the protein.
8. Kennis J.T.M., Larsen D.S., Ohta K., Facciotti M.T., Glaeser R.M., and Fleming G.R. Ultrafast protein dynamics of bacteriorhodopsin probed by photon echo and transient absorption spectroscopy. J Phys Chem B 106 (2002) 6067-6080
9. Anderson S., Dragnea V., Masuda S., Ybe J., Moffat K., and Bauer C. Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides. Biochemistry 44 (2005) 7998-8005
10. Masuda S., Hasegawa K., Ishii A., and Ono T. Light-induced structural changes in a putative blue-light receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of Synechocystis sp PCC6803. Biochemistry 43 (2004) 5304-5313
11. Masuda S., and Bauer C.E. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110 (2002) 613-623
12. Gauden M., Yeremenko S., Laan W., van Stokkum I.H.M., Ihalainen J.A., van Grondelle R., Hellingwerf K.J., and Kennis J.T.M. Photocycle of the flavin-binding photoreceptor AppA, a bacterial transcriptional antirepressor of photosynthesis genes. Biochemistry 44 (2005) 3653-3662. The first full characterization of the early stages of the BLUF photocycle is reported from femtoseconds to milliseconds. It is shown that the red-shifted product state is formed in less than 1 ns and that no further spectral changes in the UV-vis occur up to milliseconds. A minor fraction of flavin triplet states was shown to represent a physiologically irrelevant side reaction.
13. Gauden M., van Stokkum I.H.M., Key J.M., Luhrs D.C., Van Grondelle R., Hegemann P., and Kennis J.T.M. Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor. Proc Natl Acad Sci U S A 103 (2006) 10895-10900. The photoactivation mechanism of BLUF domains was investigated by femtosecond transient absorption study with broadband white-light multichannel detection and extensive kinetic modeling. H/D exchange effects on the reaction dynamics revealed proton/hydrogen transfer steps in the photoreaction. A photocycle scheme involving anionic and neutral flavin radical intermediates was established and on basis of the BLUF crystal structure, a detailed molecular reaction mechanism was proposed.
14. Laan W., Gauden M., Yeremenko S., van Grondelle R., Kennis J.T.M., and Hellingwerf K.J. On the mechanism of activation of the BLUF domain of AppA. Biochemistry 45 (2006) 51-60
15. Dragnea V., Waegele M., Balascuta S., Bauer C., and Dragnea B. Time-resolved spectroscopic studies of the AppA blue-light receptor BLUF domain from Rhodobacter sphaeroides. Biochemistry 44 (2005) 15978-15985
16. Zirak P., Penzkofer A., Schiereis T., Hegemann P.A.J., and Schlichting I. Absorption and fluorescence spectroscopic characterization of BLUF domain of AppA from Rhodobacter sphaeroides. Chem Phys 315 (2005) 142-154
17. Gauden M., Grinstead J.S., Laan W., van Stokkum I.H.M., Avila-Perez M., Toh K.C., Boelens R., Kaptein R., van Grondelle R., Hellingwerf K.J., and Kennis J.T.M. On the role of aromatic side chains in the photoactivation of BLUF domains. Biochemistry 46 (2007) 7405-7415. Here, it is shown that electron transfer to FAD from a conserved tyrosine or a conserved tryptophan determines all photochemistry in BLUF domains. Electron transfer from tyrosine results in formation of the signaling state, while electron transfer from tryptophan provides a nonproductive deactivation pathway.
18. Grinstead J.S., Hsu S.T.D., Laan W., Bonvin A.M.J.J., Hellingwerf K.J., Boelens R., and Kaptein R. The solution structure of the AppA BLUF domain: insight into the mechanism of light-induced signaling. Chembiochem 7 (2006) 187-193
19. Masuda S., Tomida Y., Ohta H., and Takamiya K. The critical role of a hydrogen bond between Gln63 and Trp104 in the blue-light sensing BLUF domain that controls AppA activity. J Mol Biol 368 (2007) 1223-1230
20. Kennis J.T.M., Crosson S., Gauden M., van Stokkum I.H.M., Moffat K., and van Grondelle R. Primary reactions of the LOV2 domain of phototropin, a plant blue-light photoreceptor. Biochemistry 42 (2003) 3385-3392
21. Schuttrigkeit T.A., Kompa C.K., Salomon M., Rudiger W., and Michel-Beyerle M.E. Primary photophysics of the FMN binding LOV2 domain of the plant blue light receptor phototropin of Avena sativa. Chem Phys 294 (2003) 501-508
22. Kennis J.T.M., van Stokkum I.H.M., Crosson S., Gauden M., Moffat K., and van Grondelle R. The LOV2 domain of phototropin: a reversible photochromic switch. J Am Chem Soc 126 (2004) 4512-4513
23. Kotting C., and Gerwert K. Proteins in action monitored by time-resolved FTIR spectroscopy. Chem Phys Chem 6 (2005) 881-888
24. Groot M.L., Van Wilderen L.J.G.W., and Di Donato M. Femtosecond time-resolved and dispersed infrared spectroscopy on proteins. Photochem Photobiol Sci 6 (2007) 501-507. This review gives a full account of femtosecond infrared spectroscopy technique along with applications to various photobiological systems.
25. Hellingwerf K.J., Hendriks J., and Gensch T. Photoactive yellow protein, a new type of photoreceptor protein: will this "yellow lab" bring us where we want to go?. J Phys Chem A 107 (2003) 1082-1094
26. van Stokkum I.H., Larsen D.S., and van Grondelle R. Global and target analysis of time-resolved spectra. Biochim Biophys Acta 1657 (2004) 82-104
27. Ujj L., Devanathan S., Meyer T.E., Cusanovich M.A., Tollin G., and Atkinson G.H. New photocycle intermediates in the photoactive yellow protein from Ectothiorhodospira halophila: picosecond transient absorption spectroscopy. Biophys J 75 (1998) 406-412
28. Changenet-Barret P., Espagne A., Charier S., Baudin J.B., Jullien L., Plaza P., Hellingwerf K.J., and Martin M.M. Early molecular events in the photoactive yellow protein: role of the chromophore photophysics. Photochem Photobiol Sci 3 (2004) 823-829
29. Larsen D.S., van Stokkum I.H.M., Vengris M., van der Horst M.A., de Weerd F.L., Hellingwerf K.J., and van Grondelle R. Incoherent manipulation of the photoactive yellow protein photocycle with dispersed pump-dump-probe spectroscopy. Biophys J 87 (2004) 1858-1872
30. Groot M.L., van Wilderen L.J., Larsen D.S., van der Horst M.A., van Stokkum I.H., Hellingwerf K.J., and van Grondelle R. Initial steps of signal generation in photoactive yellow protein revealed with femtosecond mid-infrared spectroscopy. Biochemistry 42 (2003) 10054-10059
31. van Wilderen L.J., van der Horst M.A., van Stokkum I.H., Hellingwerf K.J., van Grondelle R., and Groot M.L. Ultrafast infrared spectroscopy reveals a key step for successful entry into the photocycle for photoactive yellow protein. Proc Natl Acad Sci U S A 103 (2006) 15050-15055. The isomerization of the p-coumaric acid chromophore in PYP was investigated by femtosecond infrared spectroscopy. Breaking of a hydrogen bond between the backbone and the chromophore was identified as a key step for successful entry into the photocycle.
32. Heyne K., Mohammed O.F., Usman A., Dreyer J., Nibbering E.T.J., and Cusanovich M.A. Structural evolution of the chromophore in the primary stages of trans/cis isomerization in photoactive yellow protein. J Am Chem Soc 127 (2005) 18100-18106. The isomerization reaction of p-coumaric acid in PYP was characterized in great detail through femtosecond IR spectroscopy in combination with quantum-chemical calculations.
33. Groenhof G., Bouxin-Cademartory M., Hess B., De Visser S.P., Berendsen H.J.C., Olivucci M., Mark A.E., and Robb M.A. Photoactivation of the photoactive yellow protein: why photon absorption triggers a trans-to-cis lsomerization of the chromophore in the protein. J Am Chem Soc 126 (2004) 4228-4233
34. Premvardhan L.L., van der Horst M.A., Hellingwerf K.J., and van Grondelle R. Stark spectroscopy on photoactive yellow protein, E46Q, and a nonisomerizing derivative, probes photo-induced charge motion. Biophys J 84 (2003) 3226-3239
35. Wagner J.R., Brunzelle J.S., Forest K.T., and Vierstra R.D. A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438 (2005) 325-331
36. Yang X., Stojkovic E.A., Kuk J., and Moffat K. Crystal structure of the chromophore-binding domain of an unusual bacteriophytochrome RpBphP3 reveals residues that modulate photoconversion. Proc Natl Acad Sci U S A 104 (2007) 12571-12576
37. 5 bond was observed at a previously considered structurally inactive part of the chromophore.
38. Kobayashi T., Saito T., and Ohtani H. Real-time spectroscopy of transition states in bacteriorhodopsin during retinal isomerization. Nature 414 (2001) 531-534
39. Herbst J., Heyne K., and Diller R. Femtosecond infrared spectroscopy of bacteriorhodopsin chromophore isomerization. Science 297 (2002) 822-825
40. Kukura P., McCamant D.W., and Mathies R.A. Femtosecond stimulated raman spectroscopy. Annu Rev Phys Chem 58 (2007) 461-488. This review provides a comprehensive overview of femtosecond-stimulated Raman spectroscopy and its application to various photoactive systems.
41. 12 double bond was found to occur in less than 200 fs. Further evolution to a strained all-trans structure took place in ∼1 ps.
42. Schoenlein R.W., Peteanu L.A., Mathies R.A., and Shank C.V. The 1st step in vision-femtosecond isomerization of Rhodopsin. Science 254 (1991) 412-415
43. McCamant D.W., Kukura P., and Mathies R.A. Femtosecond stimulated Raman study of excited-state evolution in bacteriorhodopsin. J Phys Chem B 109 (2005) 10449-10457. This paper concerns a femtosecond-stimulated Raman study on bacteriorhodopsin. Although no dynamic structural information is obtained during the first picosecond because of distortion of the signals by ground-state Raman features, evidence is provided for dissipation of Franck-Condon active modes of retinal into reactive low-frequency modes.
44. Lenz M.O., Huber R., Schmidt B., Gilch P., Kalmbach R., Engelhard M., and Wachtveitl J. First steps of retinal photoisomerization in proteorhodopsin. Biophys J 91 (2006) 255-262. Here, a first full account of the excited-state reactions of retinal in proteorhodopsin is given as probed with visible ultrafast spectroscopy. Isomerization of all-trans retinal was found to proceed in a way similar to that of bacteriorhodopsin.
45. Pollard W.T., and Mathies R.A. Analysis of femtosecond dynamic absorption spectra of nonstationary states. Annu Rev Phys Chem 43 (1992) 497-523
46. Kahan A., Nahmias O., Friedman N., Sheves M., and Ruhman S. Following photoinduced dynamics in bacteriorhodopsin with 7-fs impulsive vibrational spectroscopy. J Am Chem Soc 129 (2007) 537-546. This paper concerns a comprehensive study of impulsive vibrational spectroscopy (IVS) on bacteriorhodopsin. It is demonstrated that the IVS signals mainly arise from an impulsive stimulated Raman process creating wavepackets on the ground-state potential energy surface, and thus limited information on excited-state dynamics is obtained.