Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET

Subscriber access provided by Nottingham Trent University

B: Biophysics; Physical Chemistry of Biological Systems and Biomolecules

Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET Mechanisms in Photosystem I Oleg G. Poluektov, Jens Niklas, and Lisa M. Utschig J. Phys. Chem. B, Just Accepted Manuscript • DOI: 10.1021/acs.jpcb.9b06636 • Publication Date (Web): 12 Aug 2019 Downloaded from pubs.acs.org on August 12, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

The Journal of Physical Chemistry

Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET Mechanisms in Photosystem I

Oleg G. Poluektov*, Jens Niklas, Lisa M. Utschig* †

Chemical Sciences and Engineering Division, Argonne National Laboratory, 9700 S. Cass Ave., Lemont, IL 60439, USA, *To whom correspondence should be addressed. E-mail: [email protected]; [email protected]

1 ACS Paragon Plus Environment

The Journal of Physical Chemistry 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Abstract Following light-generated electron transfer reactions in photosynthetic reaction center proteins, an entangled spin qubit (radical) pair is created. The exceptional sensitivity of entangled quantum spin states to weak magnetic interactions, structure, and local environments was used to monitor the directionality of electron transfer in Photosystem I (PSI). EPR spectra of radical pairs formed via each symmetric branch of cofactors, A or B, exhibit distinctive line shapes. By photochemical reduction and biochemical modification of PSI we created samples where the radical pair(s) from (1) only A-branch, (2) only B-branch, or (3) both A- and B-branches are detectable. These PSI samples were used to analyze the asymmetry of electron transfer as a function of temperature, freezing condition, and temperature cycling. The temperature dependency agrees with a dynamic model in which the conformational states of the protein regulate the directionality of electron transfer. High spectral resolution afforded by high frequency (130 GHz) EPR, combined with extra resolution afforded by deuterated proteins, provides new mechanistic insight via structural and environmental sensitivity of the entangled electron spins of photogenerated radical pairs.


Page 2 of 21

Page 3 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


INTRODUCTION Natural photosynthetic systems efficiently capture and convert solar energy, storing the energy in the chemical bonds of carbohydrates.1-2 The key light-induced reactions occur in photosynthetic reaction center (RC) proteins with near unity quantum efficiency. To date, artificial solar energy conversion systems cannot achieve this high efficiency. Resolving fundamental mechanisms of photochemical energy conversion in photosynthetic RCs provides significant insights useful for improving the design and efficiency of man-made photosynthetic devices.3-7 Photosynthetic RCs are integral transmembrane protein-cofactor complexes in which light-initiated rapid, sequential electron transfer (ET) result in the formation of stabilized charge separation across the membrane, which is then used to drive subsequent chemical reactions of photosynthesis.1-2, 8-10 The ET events occur through a RC protein-embedded chain of electron donor and acceptor molecules. There are two types of RCs, Type I and Type II, as defined by their terminal electron acceptor cofactors. Photosystem I (PSI) and Photosystem II (PSII) are central representatives of each class. X-ray studies of photosynthetic RC single crystals reveal a similar structural arrangement, each containing two branches of cofactors arranged in a pseudo two-fold symmetry and referred to as the A and B branches (Figure 1).11-17 Each branch consists of the primary electron donor P (a dimer of chlorophyll molecules), two chlorin molecules and one quinone. It is well established that ET in Type II RCs is asymmetric, with only the A-branch active.8, 10, 18

This unidirectional nature of ET can be rationalized by the different functions of the quinones

in A- and B- branches. Upon initial excitation of the primary donor P, one electron transfers to an intermediate electron acceptor IA, a pheophytin molecule, with subsequent transfer to the primary quinone acceptor QA (Figure 1a). This sequence of electron transfer steps results in stabilization of a transient charge-separated state in the form of the coulombic coupled radical ion-pair P+QA-. Electron transfer terminates with interquinone electron transfer to the terminal quinone acceptor QB located in the B-branch. After a two-electron, two-proton reduction, QBH2 is released from RC for further chemical transformations.1, 8, 10 In contrast, neither of the two quinone molecules in Type I RCs, termed A1A and A1B, acts as terminal electron acceptor, but sequential ET continues to three [4Fe-4S] clusters termed FX, FA, and FB (Figure 1b).9, 19-20 The ET in the Type I RC like PSI was presumed for a long time to be unidirectional by analogy to Type II RCs, despite no different functionality of the quinones A1A and A1B. According to the primary paradigm, ET in PSI occurs only along the A-branch and is blocked at low temperatures beyond A1A quinone.19-20 This model is in good agreement with time-resolved 3 ACS Paragon Plus Environment


(TR) EPR data, where only one type of short-lived radical pair (RP), namely P+A-1A, has been observed.20-22 However, EPR spectra from PSI illuminated at low temperature always reveal strong stable signals of P+ and reduced [4Fe-4S] clusters, which is direct proof of ET from P to FX, FA, and FB at low temperature.9, 20, 23-27 This was originally explained within the unidirectional model as ET occurring via the A-branch in partially damaged RCs or RCs in a different conformational state. In contrast, we suggested that this ET does not occur via A-branch but through the B-branch, where the electrons do not stop at the quinone with the RP P+A-1B but proceed further to FX, FA, and FB.21 At low temperature, [4Fe-4S] clusters are deep traps for electrons and thus electron recombination to the oxidized primary donor P+ is largely suppressed. Therefore, at low temperatures, where most of the TR-EPR experiments were done, transient RP in Type I RCs is observed only in the A-branch.20-22

Figure 1. Schematic structure and ET pathways in photosynthetic RCs of Type II (a), Type I (b), and Type I with iron-sulfur complexes removed (c). The donor and acceptor cofactors in Type II and Type I photosynthetic RCs are arranged in two symmetric branches, A (red) and B (blue). a) Type II bacterial RC from Rhodobactor sphaeroides. The primary donor P is a pair of bacteriochlorophyll molecules. The intermediate acceptors IA/B are bacteriopheophytins, and the terminal acceptors QA/B are ubiquinone molecules positioned around a non-heme Fe ion. The unidirectional ET pathway is indicated by arrows. After a twoelectron, two-proton reduction QBH2 is released from the RC, transporting electrons and protons to other redox components in the bacteria. b) Type I Photosystem I (PSI) RC from cyanobacterium. Following photoexcitation, the primary donor P becomes oxidized, transferring its electron to one of two identical chains of donor/acceptor molecules: a chlorophyll A 0, phylloquinone A1, and three [4Fe-4S] clusters, FX, FA, and FB. Photoinduced ET in PSI is bidirectional, proceeding through both the A- and B-branches of cofactors as indicated by arrows. c) Type I RC, same as b), with iron-sulfur complexes removed. ET cannot proceed past the quinones A1A/B.

The unidirectional model for ET in PSI was first questioned following results obtained from optical studies of quinone reoxidation kinetics.28 Bi-exponential room temperature decay kinetics


Page 4 of 21

Page 5 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


with almost equal pre-exponential coefficients were interpreted as back ET from both A1A and A1B quinones, thus suggesting a bidirectional ET model for PSI. This publication spurred a series of time-resolved (TR) optical and EPR studies of both native PSI and site-directed mutants of PSI in which one of the cofactor branches was selectively blocked or disrupted. Several of these early publications support the unidirectional model, whereas others favor bidirectional ET.29-35 Inherent limitations of optical and conventional TR-EPR techniques make interpretation of the published results ambiguous due to the lack of a direct correlation of kinetic and structural data, i.e. which spectroscopic signature can be assigned with certainty to a particular cofactor in PSI. To overcome this problem, we used high frequency (HF), time-resolved EPR spectroscopy to investigate the question of directionality in PSI.36-37 For photosynthetic RCs, TR-EPR signals are recorded after pulsed laser excitation, which initiates ET to generate one or more sequential radical-ion pairs (RPs), each having four distinct energy levels depending on the orientation of the cofactors with respect to the external magnetic field (Figure S1). At high field/high frequency EPR, like D-band (130 GHz, 4.6 T), the interactions between the cofactor radicals P+ and A1(distance  25 Å) are small in comparison to the differences in resonance frequencies of the radicals; this is the so-called weak coupling limit (see SI). It is important to note, that this weak coupling limit is typically not a good approximation at conventional EPR frequencies like X-band (9.5 GHz, 0.34 T). Created from an excited singlet state of the donor, these spins are initially entangled or correlated with relatively long correlation time allowing them to be detected by TREPR. These entangled states are observed in RCs and termed spin-correlated radical pairs (SCRP).25,

38-40

A single electron spin can be considered as a classical qubit in quantum

information science. SCRP is thus an entangled two spin qubit system and is of great interest in quantum information and quantum sensing applications.41-44 The SCRP spectra observed for RCs at HF are exceptionally sensitive to weak magnetic interactions, structure and heterogeneous local protein environments and reveal strong non-Boltzmann electron polarization (see SI and refs

36, 38-39, 45-48

). These phenomena result in line shapes different from the RP spectra in

equilibrium and consist of a series of antiphase doublets, i.e. alternation of emissive and absorptive lines (Figure 2 and SI).49-50 Thus, using SCRPs as quantum sensors we were able to connect kinetics of back ET from the quinones A-1A and A-1B to the primary donor P+ by resolving



Page 6 of 21

the structure of two distinct radical pairs, P+A1A

and P+A-1B and, thus, prove bidirectional ET

in PSI (Figure 3, SI Figure 1d,f).21 To obtain these data we employed established methods for blocking forward ET in PSI beyond A1. While FA and FB can be easily reduced chemically, reduction of FX can be achieved only by pre-illumination of already chemically reduced PSI samples followed by rapid freezing to 100 K or lower.51 This procedure also reduces A1A but not A1B. Figure 2. High frequency (130 GHz) pulsed EPR spectra of the P+A-1A radical pair in the thermal equilibrium (top, purple) and in spin-polarized SCRP state (bottom, red) at 100 K. Green and blue spectra are the simulations for A1Aand P+ EPR spectra in thermal equilibrium, respectively. Positions of the g-tensor main components for A1A- and P+ are shown by arrows. SCRP spectrum was detected with 2 s delay after laser flash. Note, that EPR spectra recorded in pulsed mode are exhibiting absorptive-type line shapes and not derivative-type line shapes as typically seen in continuous wave EPR. The overlap of absorptive and emissive lines (antiphase doublets) in the SCRP results in the appearance of derivative-type line shapes (see SI for details).

By

increasing

the

length

of

the

pre-

illumination time and thus the degree of [4Fe4S] cluster reduction, we observed a gradual change in the TR-EPR spectra and changes in back recombination rates from 60 s to 6 s (Figure 3 and SI). This transformation corresponds to the changes of RP geometry from P+A-1A (60 s recombination) to P+A-1B (6 s

recombination)

as

established

by

comparison with the X-ray crystal structure11 of PSI (see SI, Figure S1f). Thus for the first time we could correlate the radical pair recombination kinetics with its geometry which provides direct evidence of the nowadays well-accepted bidirectionality of ET in PSI.20,

24, 26, 52-57

Note, that

conventional EPR at lower microwave frequencies such as X-band in principle also contains the same structure information, however the unique identification of the structure is obscured mainly owing to lower spectral resolution and non-validity of weak coupling limit at low magnetic field.39


Page 7 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


A potential drawback of this experimental approach is that the strong reducing conditions could, in principle, result in re-direction of ET from one branch to the other. It also makes determining the degree of ET asymmetry along A- and B-branches impossible, i.e. the relative yield of the two branches. According to several recent publications, the A-branch is the dominant channel for ET in PSI, with reported ratios for A/B ET ranging from 90/10 to 50/50.20, 24, 26, 35, 53, 5859

The bulk of these results were obtained with optical studies of site-directed RC mutants and

should be taken with care as mutagenesis may also influence the asymmetry of the ET.

Figure 3. Experimental 130 GHz TR-EPR spectra of PSI complexes from fully deuterated cyanobacterium Synechococcus leopoliensis and schematic structure of ET pathways in PSI.21,22 SCRP spectra recorded at 100 K, delay after laser flash, DAF-time 1 s. Red, right - spectrum from intact native PSI. A-branch ET is blocked beyond quinone A1A. B-branch ET is irreversible and terminated at iron-sulfur complexes FA/B. Blue, left - spectrum from biochemically modified PSI RCs wherein the terminal acceptor iron-sulfur centers, FA/FB and FX have been removed in order to block ET beyond A1 quinones. This sample was treated with sodium hydrosulfite and pre-illuminated at 205-245 K for 1 hr prior to data collection. This reduction procedure reduces the A 1A quinone, thus preventing ET along A branch. Bottom, black – spectrum from biochemically modified PSI RCs wherein the terminal acceptor iron-sulfur centers, FA/FB and FX have been removed; no prereduction conditions. In both A- and B-branches ET is blocked beyond quinone acceptors A1A/B. Bottom, purple - spectrum is a sum of two spectra: 44% of (P+A1A-, red spectrum) + 56% of (P+A1B-, blue spectrum).

To overcome this problem, we examined the extent of A- vs B-branch ET in PSI core complexes where FX, FA and FB were removed to prevent forward ET from the quinones to the [4Fe-4S] clusters.22 We observed a TR-EPR spectrum at 100 K comprised of two overlapping signals: one from SCRP in the A-branch, P+A-1A, and another from SCRP formed in the B-branch, P+A-1B, with an almost equal ratio of ET through A- and B-branches (Figure 3, Figure S3, and SI). 7 ACS Paragon Plus Environment


These results were possible due to two essential features of the experimental design: deuteration of PSI, which improves the spectral resolution by decreasing the EPR linewidth, and the high resolution afforded by HF (130 GHz) TR-EPR. A very important question remains: What is the mechanism responsible for regulating the pathway the electron chooses to take? Two general models are conceivable. First, ET along Aor B-branch could be a purely stochastic process, i.e. upon light excitation there is a fixed probability that the electron will travel down either one or another branch. Second, the pathway could be predetermined for a particular RC, i.e. by preparation, or natural evolution one population of RCs utilizes only the A-branch for ET whereas the other population is only capable of B-branch ET. Herein, we clarify this issue by examining the ratio of ET between the A- and B-branches as a function of temperature. MATERIALS AND METHODS Sample preparation. PSI reaction centers were extracted from 99% deuterated cyanobacterium Synechococcus leopoliensis

60

as described in

61

Purified PSI was prepared in 50 mM MES, pH

6.5, 20% glycerol, 0.03% β-DM (n-dodecyl β-D-maltopyranoside, Anatrace), 30 mM sodium ascorbate. The [4Fe-4S] clusters were removed by established preparations. PSI (0.2 mg Chl/ml) was incubated in a buffer containing 6.8 M urea, 62 mM Tris, 76 mM glycine-NaOH, pH 10, for 1 h, as previously described to remove FA/FB.62 The PSI sample was then dialyzed overnight against 50 mM Tris-HCl pH 8.3. To remove FX, the sample was further treated with 3 M urea, 5 mM K3FeCN6, 50 mM Tris-HCl, pH 8.0, for 4.5 h.63 The PSI sample was dialyzed overnight against 50 mM Tris-HCl, pH 8.3, and 5 mM 4,5-dihydroxy-1,3-benzene-disulfonic acid (disodium salt), and then again overnight against 2 changes of 50 mM Tris-HCl, pH 8.0, 0.03% β-DM. The sample, analyzed by ICP-AES, showed a ratio of ~1 Fe/PSI monomer after urea treatment, confirming removal of the three [4Fe-4S] clusters. For EPR, the Fe-removed PSI sample was concentrated to 150 µM PSI monomer with final conditions of 50 mM Tris-Cl, pH 8.3, 20% glycerol, 0.03% βDM, and 10 mM sodium ascorbate. Chemically reduced Fe-removed PSI samples were prepared in 50 mM glycine-KOH pH 9.87, 20 % glycerol, 0.03% β-DM and 40 mM sodium hydrosulfite. Chemically reduction in combination with photochemical reduction was accomplished by treating PSI samples with either 0.1 M sodium ascorbate in 50 mM MES-NaOH buffer, pH 6, or 0.2 M sodium hydrosulfite in 2 M glycine-KOH buffer, pH 10. Final reductant concentrations were ~10 mM for sodium ascorbate and ~40 mM for sodium hydrosulfite. All samples were dark-adapted for ~15 minutes at room temperature. This procedure leads to the reduction of FA and FB iron8 ACS Paragon Plus Environment

Page 8 of 21

Page 9 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


sulfur complexes in the sodium hydrosulfite containing samples. The reduction of FX and A1A was achieved by illumination of these samples at 205-245 K followed by rapid freezing to 100 K. The samples were loaded into quartz tubes (inner diameter 0.5 mm / outer diameter 0.6 mm), dark-adapted, and placed in the microwave cavity. The cavity was held in an Oxford flow cryostat, and temperature was controlled by the Oxford temperature control system. Sodium ascorbate containing samples were cooled down to 100 K in the dark. Sodium hydrosulfite containing samples were cooled down to 205 – 245 K in the dark, followed by illumination for various time durations with laser light. EPR spectroscopy. EPR measurements were performed on a pulsed/continuous wave high frequency D-band (130GHz/4.6T) EPR spectrometer37, 64 with single mode cylindrical cavity TE011. Pulsed TR-EPR spectra of the spin-correlated radical pairs (SCRP) were recorded by monitoring the electron spin echo (ESE) intensity from a two microwave pulse sequence, which followed a short ( Phe Mutants of Photosystem I. Appl. Magn. Reson. 2010, 38, 187-203.


Page 18 of 21

Page 19 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


(56) Berthold, T.; von Gromoff, E. D.; Santabarbara, S.; Stehle, P.; Link, G.; Poluektov, O. G.; Heathcote, P.; Beck, C. F.; Thurnauer, M. C.; Kothe, G. Exploring the Electron Transfer Pathways in Photosystem I by High-Time-Resolution Electron Paramagnetic Resonance: Observation of the B-Side Radical Pair P700+A1- in Whole Cells of the Deuterated Green Alga Chlamydomonas reinhardtii at Cryogenic Temperatures. J. Am. Chem. Soc. 2012, 134, 5563-5576. (57) McConnell, M. D.; Sun, J. L.; Siavashi, R.; Webber, A.; Redding, K. E.; Golbeck, J. H.; van der Est, A. Species-Dependent Alteration of Electron Transfer in the Early Stages of Charge Stabilization in Photosystem I. Biochim. Biophys. Acta 2015, 1847, 429-440. (58) Bautista, J. A.; Rappaport, F.; Guergova-Kuras, M.; Cohen, R. O.; Golbeck, J. H.; Wang, J. Y.; Beal, D.; Diner, B. A. Biochemical and Biophysical Characterization of Photosystem I from Phytoene Desaturase and ζ-Carotene Desaturase Deletion Mutants of Synechocystis sp PCC 6803. J. Biol. Chem. 2005, 280, 20030-20041. (59) Cherepanov, D. A.; Milanovsky, G. E.; Gopta, O. A.; Balasubramanian, R.; Bryant, D. A.; Semenov, A. Y.; Golbeck, J. H. Electron-Phonon Coupling in Cyanobacterial Photosystem I. J. Phys. Chem. B 2018, 122, 7943-7955. (60) Daboll, H. F.; Crespi, H. L.; Katz, J. J. Mass cultivation of algae in pure heavy water. Biotechnol. Bioeng. 1962, 4, 218. (61) Utschig, L. M.; Chen, L. X.; Poluektov, O. G. Discovery of Native Metal Ion Sites Located on the Ferredoxin Docking Side of Photosystem I. Biochemistry 2008, 47, 3671-3676. (62) Parret, K. G.; Mehari, T.; Warren, P. G.; Golbeck, J. H. Purification and Properties of the Intact P700 and Fx-Containing Photosystem I Core Protein. Biochem. Biophys. Acta 1989, 973, 324. (63) Warren, P. V.; Parrett, K. G.; Warden, J. T.; Golbeck, J. H. Characterization of a Photosystem I Core Containing P700 and Intermediate Electron Acceptor A1. Biochemistry 1990, 29, 6545-6550. (64) Bresgunov, A. Y.; Dubinskii, A. A.; Krimov, V. N.; Petrov, Y. G.; Poluektov, O. G.; Lebedev, Y. S. Pulsed EPR in 2 mm Band. Appl. Magn. Reson. 1991, 2, 715-728. (65) Müller, M. G.; Niklas, J.; Lubitz, W.; Holzwarth, A. R. Ultrafast Transient Absorption Studies on Photosystem I Reaction Centers from Chlamydomonas reinhardtii. 1. A New Interpretation of the Energy Trapping and Early Electron Transfer Steps in Photosystem I. Biophys. J. 2003, 85, 3899-3922. (66) Holzwarth, A. R.; Müller, M. G.; Niklas, J.; Lubitz, W. Ultrafast Transient Absorption Studies on Photosystem I Reaction Centers from Chlamydomonas reinhardtii. 2: Mutations Near the P700 Raction Center Chlorophylls Provide New Insight into the Nature of the Primary Electron Donor. Biophys. J. 2006, 90, 552-565. (67) Holzwarth, A. R.; Müller, M. G.; Niklas, J.; Lubitz, W. Charge Recombination Fluorescence in Photosystem I Reaction Centers from Chlamydomonas reinhardtii. J. Phys. Chem. B 2005, 109, 5903-5911. (68) Müller, M. G.; Slavov, C.; Luthra, R.; Redding, K. E.; Holzwarth, A. R. Independent Initiation of Primary Electron Transfer in the Two Branches of the Photosystem I Reaction Center. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 4123-4128. (69) LeBard, D. N.; Kapko, V.; Matyushov, D. V. Energetics and Kinetics of Primary Charge Separation in Bacterial Photosynthesis. J. Phys. Chem. B 2008, 112, 10322-10342. (70) Popov, I.; Greenbaum, A.; Sokolov, A. P.; Feldman, Y. The Puzzling First-Order Phase Transition in Water-Glycerol Mixtures. Phys. Chem. Chem. Phys. 2015, 17, 18063-18071. (71) Ringe, D.; Petsko, G. A. The 'Glass Transition' in Protein Dynamics: What it is, Why it occurs, and How to Exploit it. Biophys. Chem. 2003, 105, 667-680. (72) Rasmussen, D. H.; MacKenzie, A. P. Glass Transition in Amorphous Water. Application of the Measurements to Problems Arising in Cryobiology. The Journal of Physical Chemistry 1971, 75, 967-973. (73) Vitkup, D.; Ringe, D.; Petsko, G. A.; Karplus, M. Solvent Mobility and the Protein 'Glass' Transition. Nat. Struct. Biol. 2000, 7, 34-38.



(74) Richert, R. Heterogeneous Dynamics in Liquids: Fluctuations in Space and Time. J. Phys.: Condens. Matter 2002, 14, R703-R738. (75) Utschig, L. M.; Tiede, D. M.; Poluektov, O. G. Light-Induced Alteration of Low-Temperature Interprotein Electron Transfer between Photosystem I and Flavodoxin. Biochemistry 2010, 49, 9682-9684.


Page 20 of 21

Page 21 of 21 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


TOC Graphics


Spin-Correlated Radical Pairs as Quantum Sensors of Bidirectional ET

Recommend Documents