Ultrafast Photochemical Reaction of Exiguobacterium sibiricum Rhodopsin (ESR) at Alkaline pH

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Acesso é pago ou somente para assinantes

Resumo

Rhodopsin from the eubacterium Exiguobacterium sibiricum (ESR) performs the function of light-dependent proton transport. The operation of ESR is based on the ultrafast photochemical reaction of isomerization of the retinal chromophore, which triggers dark processes closed in the photocycle. Many parameters of the photocycle are determined by the degree of protonation of Asp85 – the primary counterion of the chromophore group and the proton acceptor. ESR in detergent micelles pumps protons most efficiently at pH > 9, when Asp85 is almost completely deprotonated. In this work, the photochemical reaction of ESR at pH 9.5 was studied by femtosecond laser absorption spectroscopy. It was shown that photoisomerization of the chromophore group occurs in 0.51 ps, and the contribution of the reactive excited state is about 80%. A comparison with the data we obtained at pH 7.4 showed that at pH 9.5 the reaction proceeds much faster and more efficiently. The data obtained confirm the important role of the chromophore group counterion in the photoactivated processes of rhodopsins.

Texto integral

Acesso é fechado

Sobre autores

O. Smitienko

Emanuel Institute of Biochemical Physics

Autor responsável pela correspondência
Email: djolia@gmail.com
Rússia, ul. Kosygina 4, Moscow, 119334

T. Feldman

Emanuel Institute of Biochemical Physics; Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

Rússia, ul. Kosygina 4, Moscow, 119334; Leninskie gory 1, Moscow, 119991

L. Petrovskaya

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: djolia@gmail.com
Rússia, ul. Mikluho-Maklaya 16/10, Moscow, 117997

E. Kryukova

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: djolia@gmail.com
Rússia, ul. Mikluho-Maklaya 16/10, Moscow, 117997

I. Shelaev

Semenov Federal Research Center of Chemical Physics

Email: djolia@gmail.com
Rússia, ul. Kosygina 4, Moscow, 119991

F. Gostev

Semenov Federal Research Center of Chemical Physics

Email: djolia@gmail.com
Rússia, ul. Kosygina 4, Moscow, 119991

D. Cherepanov

Semenov Federal Research Center of Chemical Physics

Email: djolia@gmail.com
Rússia, ul. Kosygina 4, Moscow, 119991

I. Kolchugina

Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

Rússia, Leninskie gory 1, Moscow, 119991

D. Dolgikh

Emanuel Institute of Biochemical Physics; Lomonosov Moscow State University; Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: djolia@gmail.com

Department of Biology

Rússia, ul. Kosygina 4, Moscow, 119334; Leninskie gory 1, Moscow, 119991; ul. Mikluho-Maklaya 16/10, Moscow, 117997

V. Nadtochenko

Semenov Federal Research Center of Chemical Physics

Email: djolia@gmail.com
Rússia, ul. Kosygina 4, Moscow, 119991

M. Kirpichnikov

Lomonosov Moscow State University; Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

Email: djolia@gmail.com

Department of Biology

Rússia, Leninskie gory 1, Moscow, 119991; ul. Mikluho-Maklaya 16/10, Moscow, 117997

M. Ostrovsky

Emanuel Institute of Biochemical Physics; Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

Rússia, ul. Kosygina 4, Moscow, 119334; Leninskie gory 1, Moscow, 119991

Bibliografia

  1. Ernst O.P., Lodowski D.T., Elstner M., Hegemann P., Brown L.S., Kandori H. // Chem. Rev. 2014. V. 114. P. 126−163. https://doi.org/10.1021/cr4003769
  2. Balashov S.P., Petrovskaya L.E., Lukashev E.P., Imasheva E.S., Dioumaev A.K., Wang J.M., Sychev S.V., Dolgikh D.A., Rubin A.B., Kirpichnikov M.P., Lanyi J.K. // Biochemistry. 2012. V. 51. P. 5748−5762. https://doi.org/10.1021/bi300409m
  3. Dioumaev A.K., Petrovskaya L.E., Wang J.M., Balashov S.P., Dolgikh D.A., Kirpichnikov M.P., Lanyi J.K. // J. Phys. Chem. B. 2013. V. 117. P. 7235− 7253. https://doi.org/10.1021/jp402430w
  4. Petrovskaya L.E., Lukashev E.P., Chupin V.V., Sychev S.V., Lyukmanova E.N., Kryukova E.A., Ziganshin R.H., Spirina E.V., Rivkina E.M., Khatypov R.A., Erokhina L.G., Gilichinsky D.A., Shuvalov V.A., Kirpichnikov M.P. // FEBS Lett. 2010. V. 584. P. 4193−4196. https://doi.org/10.1016/j.febslet.2010.09.005
  5. Balashov S.P., Petrovskaya L.E., Imasheva E.S., Lukashev E.P., Dioumaev A.K., Wang J.M., Sychev S.V., Dolgikh D.A., Rubin A.B., Kirpichnikov M.P., Lanyi J.K. // J. Biol. Chem. 2013. V. 288. P. 21254−21265. https://doi.org/10.1074/jbc.M113.465138
  6. Siletsky S.A., Mamedov M.D., Lukashev E.P., Balashov S.P., Dolgikh D.A., Rubin A.B., Kirpichnikov M.P., Petrovskaya L.E. // Biochim. Biophys. Acta. Bioenerg. 2016. V. 1857. P. 1741−1750. https://doi.org/10.1016/j.bbabio.2016.08.004
  7. Smitienko O.A., Feldman T.B., Petrovskaya L.E., Nekrasova O.V., Yakovleva M.A., Shelaev I.V., Gostev F.E., Cherepanov D.A., Kolchugina I.B., Dolgikh D.A., Nadtochenko V.A., Kirpichnikov M.P., Ostrovsky M.A. // J. Phys. Chem. B. 2021. V. 125. P. 995–1008. https://doi.org/10.1021/acs.jpcb.0c07763
  8. Arlt T., Schmidt S., Zinth W., Haupts U., Oesterhelt D. // Chem. Phys. Lett. 1995. V. 241. P. 559−565. https://doi.org/10.1016/0009-2614(95)00664-P
  9. Wand A., Loevsky B., Friedman N., Sheves M., Ruhman S. // J. Phys. Chem. B. 2013. V. 117. P. 4670− 4679. https://doi.org/10.1021/jp309189y
  10. Inoue K., Tahara S., Kato Y., Takeuchi S., Tahara T., Kandori H. // J. Phys. Chem. B. 2018. V. 122. P. 6453– 6461. https://doi.org/10.1021/acs.jpcb.8b01279
  11. Tahara S., Takeuchi S., Abe-Yoshizumi R., Inoue K., Ohtani H., Kandori H., Tahara T. // J. Phys. Chem. B. 2018. V. 122. P. 4784−4792. https://doi.org/10.1021/acs.jpcb.8b01934
  12. Chang C.-F., Kuramochi H., Singh M., Abe-Yoshizumi R., Tsukuda T., Kandori H., Tahara T. // Phys. Chem. Chem. Phys. 2019. V. 21. P. 25728−25734. https://doi.org/10.1039/C9CP04991F
  13. Chang C.-F., Kuramochi H., Singh M., Abe-Yoshizumi R., Tsukuda T., Kandori H., Tahara T. // Chem. Int. Ed. 2022. V. 61. P. e202111930. https://doi.org/10.1002/anie.202111930
  14. McCamant D.W., Kukura P., Mathies R.A. // J. Phys. Chem. B. 2005. V. 109. P. 10449−10457. https://doi.org/10.1021/jp050095x
  15. Yu J.K., Liang R., Liu F., Martinez T.J. // J. Am. Chem. Soc. 2019. V. 141. P. 18193−18203. https://doi.org/10.1021/jacs.9b08941
  16. Scholz F., Bamberg E., Bamann C., Wachtveitl J. // Biophys. J. 2012. V. 102. P. 2649–2657. https://doi.org/ 10.1016/j.bpj.2012.04.034
  17. Slouf V., Balashov S.P., Lanyi J.K., Pullerits T., Polivka T. // Chem. Phys. Lett. 2011. V. 516. P. 96−101. https://doi.org/10.1016/j.cplett.2011.09.062
  18. Iyer E.S.S., Misra R., Maity A., Liubashevski O., Sudo Y., Sheves M., Ruhman S. // J. Am. Chem. Soc. 2016. V. 138. P. 12401−12407. https://doi.org/10.1021/jacs.6b05002
  19. Gozem S., Luk H.L., Schapiro I., Olivucci M. // Chem. Rev. 2017. V. 117. P. 13502−13565. https://doi.org/10.1021/acs.chemrev.7b00177
  20. Gozem S., Johnson P.J.M., Halpin A., Luk H.L., Morizumi T., Prokhorenko V.I., Ernst O. P., Olivucci M., Miller R.J.D. // J. Phys. Chem. Lett. 2020. V. 11. 3889−3896. https://doi.org/10.1021/acs.jpclett.0c01063
  21. Kiefer H.V., Gruber E., Langeland J., Kusochek P.A., Bochenkova A.V., Andersen L.H. // Nat. Commun. 2019. V. 10. P. 1210. https://doi.org/10.1038/s41467-019-09225-7
  22. Zgrablic G., Novello A.M., Parmigiani F. // J. Am. Chem. Soc. 2012. V. 134. P. 955−961. https://doi.org/10.1021/ja205763x
  23. Govindjee R., Balashov S.P., Ebrey T.G. // Biophys. J. 1990. V. 58. P. 597−608. https://doi.org/10.1016/S0006-3495(90)82403-6
  24. Koyama Y., Kubo K., Komori M., Yasuda H., Mukai Y. // Photochem. Photobiol. 1991. V. 54. P. 433−443. https://doi.org/10.1111/j.1751-1097.1991.tb02038.x
  25. Doig S.J., Reid P.J., Mathies R.A. // J. Phys. Chem. 1991. V. 95. P. 6372−6379. https://doi.org/10.1021/j100169a054
  26. Shim S., Dasgupta J., Mathies R.A. // J. Am. Chem. Soc. 2009. V. 131. P. 7592−7597. https://doi.org/10.1021/ja809137x
  27. Huber R., Kohler T., Lenz M.O., Bamberg E., Kalmbach R., Engelhard M., Wachtveitl J. // Biochemistry. 2005. V. 44. P. 1800−1806. https://doi.org/10.1021/bi048318h
  28. Amsden J.J., Kralj J.M., Chieffo L.R., Wang X., Erramilli S., Spudich E.N., Spudich J.L., Ziegler L.D., Rothschild K.J. // J. Phys. Chem. B. 2007. V. 111. P. 11824−11831. https://doi.org/10.1021/jp073490r
  29. Hasson K.C., Gai F., Anfinrud P.A. // Proc. Natl. Acad. Sci. USA. 1996. V. 93. P. 15124−15129. https://doi.org/10.1073/pnas.93.26.15124
  30. Kusochek P.A., Scherbinin A.V., Bochenkova A.V. // J. Phys. Chem. Lett. 2021. V. 12. P. 8664−8671. https://doi.org/10.1021/acs.jpclett.1c02312
  31. Imasheva E.S., Balashov S.P., Wang J.M., Dioumaev A.K., Lanyi J.K. // Biochemistry. 2004. V. 43. P. 1648–1655. https://doi.org/10.1021/bi0355894
  32. Menon S.T., Han M., Sakmar T.P. // Physiol. Rev. 2001. V. 81. P. 1659–1688. https://doi.org/10.1152/physrev.2001.81.4.1659
  33. Kandori H. // In: Supramolecular Photochemistry: Controlling Photochemical Processes. Chapter 14 / Eds. Ramamurthy V., Inoue Y. John Wiley & Sons, Inc., 2011. P. 571–595. https://doi.org/10.1002/9781118095300.ch14
  34. Shelaev I.V., Gostev F.E., Mamedov M.D., Sarkisov O.M., Nadtochenko V.A., Shuvalov V.A., Semenov A.Y. // Biochim. Biophys. Acta. 2010. V. 1797. P. 1410−1420. https://doi.org/10.1016/j.bbabio.2010.02.026

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
Baixar
2. Rice. 1. Photocycle ESR [3, 7].

Baixar (81KB)
Metadados
3. Fig. 2. γ-band normalized absorption spectra of dark-adapted (black curve) and light-adapted (gray curve) ESR samples in DDM with absorption maxima indicated. The figure also shows the spectrum of the excitation pulse used in the femtosecond time-resolved experiments (dashed curve).

Baixar (107KB)
Metadados
4. Fig. 3. (a) – Differential spectra of photoinduced absorption ESR in DDM, recorded at delay times of –0.15 (1), 0.1 (2), 0.18 (3), 0.5 (4), 1 (5), 2 (6) and 20 (7) ps. In the spectral regions of the excitation pulse (λₘₐₓ = 523 nm) and the initial femtosecond pulse (λₘₐₓ = 802 nm) the data are not shown due to the intense light scattering signal; (b) – kinetic curves of photoinduced absorption ESR in DDM, recorded at probing wavelengths of 460 (1), 550 (2), 600 (3) and 850 (4) nm. For delay times up to 3 ps, the scale is linear, then – logarithmic. Model exponential curves (dashed curves) are also shown.

Baixar (216KB)
Metadados
5. Fig. 4. Structure of potential energy surfaces ESR demonstrating the decay path of the reactive excited state. The reaction coordinate is represented by the reactive vibrational modes, all-trans, 13-cis and intermediate forms of RPSB are marked. FC is the Franck-Condon state, CI is the conical intersection.

Baixar (121KB)
Metadados

Declaração de direitos autorais © Russian Academy of Sciences, 2024