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

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Abstract

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.

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About the authors

O. A. Smitienko

Emanuel Institute of Biochemical Physics

Author for correspondence.
Email: djolia@gmail.com
Russian Federation, ul. Kosygina 4, Moscow, 119334

T. B. Feldman

Emanuel Institute of Biochemical Physics; Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

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

L. E. Petrovskaya

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

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

E. A. Kryukova

Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry

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

I. V. Shelaev

Semenov Federal Research Center of Chemical Physics

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

F. E. Gostev

Semenov Federal Research Center of Chemical Physics

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

D. A. Cherepanov

Semenov Federal Research Center of Chemical Physics

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

I. B. Kolchugina

Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

Russian Federation, Leninskie gory 1, Moscow, 119991

D. A. Dolgikh

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

Email: djolia@gmail.com

Department of Biology

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

V. A. Nadtochenko

Semenov Federal Research Center of Chemical Physics

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

M. P. Kirpichnikov

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

Email: djolia@gmail.com

Department of Biology

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

M. A. Ostrovsky

Emanuel Institute of Biochemical Physics; Lomonosov Moscow State University

Email: djolia@gmail.com

Department of Biology

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

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Supplementary files

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2. Rice. 1. Photocycle ESR [3, 7].

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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).

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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.

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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.

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