Anomalous temperature dependence of the triplet-triplet energy transfer in Cereibacter sphaeroides I(L177)H mutant reaction centers

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Abstract

In photosynthetic reaction centers, quenching of the primary donor triplet state by energy transfer to the carotenoid molecule provides efficient suppression of singlet-excited oxygen generation, the potent chemical oxidant. This process in the Cereibacter sphaeroides reaction centers is thermoactivated, and discontinues at temperatures below 40 K. In these reaction centers, substitution of amino acid residue isoleucine for hystidine at the 177 position of the L-subunit results in a sharp decrease of the activation energy, so the carotenoid triplets are populated even at 10 K. Activation energy of the T-T energy transfer was estimated as 7.5 cm−1, which is more than 10-fold lower than the activation energy of the original reaction centers. At certain temperatures the energy transfer in the mutant is decelerated, which is related to the increase of the effective distance of the triplet-triplet transfer. To our knowledge, the described mutation presents the first reaction center modification leading to a significant decrease in activation energy of T-T energy transfer to the carotenoid molecule. The I(L177)H mutant reaction centers present a considerable interest for further studies of the triplet state quenching mechanisms, and of other photophysical and photochemical processes in reaction centers of bacterial photosynthesis.

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T. Y. Fufina

Institute of Basic Biological Problems, Russian Academy of Sciences

Author for correspondence.
Email: pros@issp.serpukhov.su
Russian Federation, 142290 Pushchino, Moscow Region

L. G. Vasilieva

Institute of Basic Biological Problems, Russian Academy of Sciences

Email: pros@issp.serpukhov.su
Russian Federation, 142290 Pushchino, Moscow Region

I. B. Klenina

Institute of Basic Biological Problems, Russian Academy of Sciences

Email: pros@issp.serpukhov.su
Russian Federation, 142290 Pushchino, Moscow Region

I. I. Proskuryakov

Institute of Basic Biological Problems, Russian Academy of Sciences

Email: pros@issp.serpukhov.su
Russian Federation, 142290 Pushchino, Moscow Region

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Supplementary files

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2. Fig. 1. The location of the amino acid residue of isoleucine L177 in the structure of wild-type C. sphaeroides RC (PDB ID: 6Z02). Car is a carotenoid

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3. Fig. 2. Absorption spectra of wild-type C. sphaeroides RC (dotted line) and mutant I(L177)H (solid line), T = 100 K. The QY bands of the primary donor P lie in the region of 870-890 nm. A detailed description of the spectrum is given in Vasilieva et al. [24]

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4. 3. Effect of temperature on the EPR spectra of RC mutant I(L177)H (a) and RC wild-type (b) C. sphaeroides. (1) T = 100 K, (2) T = 40 K, (3) T = 10 K. Letters on the spectra indicate: C – lines of Car triplets, P – lines of triplets of the primary donor R. The lines are indicated only in the low-field part of the spectrum. Measurement conditions: recording of a signal in the range of 0.2–1.7 microseconds after an exciting flash, λ db = 882 nm. The arrows show the direction of absorption (A) and radiation (E) of microwave power

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5. Fig. 4. Changes in optical absorption at λ = 540 nm caused by excitation into the primary donor band (λvb = 870 nm) in an RC with a restored primary acceptor. a – RC of mutant I(L177)H; b – RC of wild type. T = 100 K. The inset shows the inverted response of the system to a 6-ns laser flash. Smooth curves represent the results of convolution of the flash signal with theoretical values and exponents. The parameters of the theoretical curves are given in the text

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6. Fig. 5. Temperature dependences of the amplitude of the low-field EPR line of the Car triplet in the RC of mutant I(L177)H (a) and wild type (b) under conditions of a photo-reduced primary QA acceptor. The dotted lines and dots represent experimental data, and the solid lines represent curves calculated using the formula A = B*exp(−Ea/kT). The best matches with the experimental dependences were obtained at Ea = 7.5 cm -1 (a); Ea = 91 cm -1 (b). The standard deviations of the noise component of the spectra are given as measurement errors.

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7. Additional materials. The appendix to the article is published on the website of the journal Biochemistry (https://biochemistrymoscow.com ).
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