Electron Transfer and Protein Dynamics in the Photosynthetic Reaction Center

McMahon, Benjamin H.; Müller, Joachim D.; Wraight, Colin A.; Nienhaus, G. Ulrich

doi:10.1016/s0006-3495(98)77964-0

Cited by 197 publications

(289 citation statements)

References 93 publications

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“…Similar long lived states have been observed by other authors for native RCs frozen under different illumination conditions (15,18,38,41,42). In principal the longer lifetime of the long lived state frozen in the light may be due to a reduced electron transfer rate for the back electron transfer reaction.…”

Section: Effects Of Protein Response On Functional Properties Of Q Bsupporting

confidence: 85%

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides

et al. 2007

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Proton ENDOR spectroscopy was used to monitor local conformational changes in bacterial reaction centers (RC) associated with the electron transfer reaction DQ B → D +• Q B −• using mutant RCs capable of photo-reducing Q B at cryogenic temperatures. The charge separated state D +• Q B −• was studied in mutant RCs formed by either (i) illuminating at low temperature (77K) a sample frozen in the dark (ground state protein conformation) or (ii) illuminating at room temperature prior to and during the freezing (charge separated state protein conformation). The charge recombination rates from the two states differed greatly (>10 6 fold) as shown previously, indicating a structural change (Paddock et al (2006) Biochemistry 45, 14032 -14042). ENDOR spectra of Q B −• from both samples (35 GHz, 77K) showed three nearly identical sets of hyperfine couplings due to exchangeable protons that were similar to those for Q B −• in native RCs indicating that in all RCs, Q B −• was located at the proximal position near the metal site. In contrast, one set of H-bond couplings was observed only in the sample frozen under illumination in which the protein can relax prior to freezing. This H-bond was assigned to an interaction between the Ser-L223 hydroxyl and Q B −• based on its absence in Ser L223 → Ala mutant RCs. The Ser-L223 hydroxyl H-bond was also observed in the native RCs frozen under illumination. Thus, part of the protein relaxation in response to light induced charge separation involves the formation of an H-bond between the OH group of Ser-L223 and the anionic semiquinone Q B −• . This proton movement serves to stabilize the charge separated state and facilitate proton transfer to reduced Q B . KeywordsB-branch; bacterial reaction center; quinone movement; bacterial photosynthesis; electron transfer; nanoswitch Conformational changes in protein structure associated with electron transfer reactions play an important role in stabilizing the resultant charge separated state and determining the rates of electron transfer (1-3). In photosynthetic bacteria, reaction centers (RCs) perform the initial photochemical reactions in photosynthesis (see e.g. 4,5) resulting in the light induced reduction of a bound quinone, Q B . The reduction of Q B clearly demonstrates the influence of conformational dynamics on electron transfer. The overall reaction is shown by the solid curves in Figure 1. The first step is the initial photochemistry, a rapid (τ = 10 -10 s) light induced electron transfer from a electron donor species D (a bacteriochlorophyll dimer) along the A-branch (one of two pseudo-symmetric pathways) through a series of acceptor molecules bacteriochlorphyll, B A , bacteriopheophytin, H A , to a tightly bound quinone, Q A ( Figure 1). This is followed by a *To whom correspondence should be addressed. Phone: (858) 534-2504, Fax: (858) , is coupled to protein dynamics as shown by several experimental observations (for a review see 9). First, the rate of reaction is dependent on protein structure as illustrated by the ef...

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Section: Effects Of Protein Response On Functional Properties Of Q Bsupporting

confidence: 85%

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides

et al. 2007

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“…types of motions needed to bring RC to TC, however, cannot be defined as dihedral or bond angles but must include a global motion of the two lobes of the kinase that compress the active site and drive the reactants together. One reason for suggesting the Agmon-Hopfield formalism rather than thermodynamic integration is our expectation, based on experiments (35,36), that relevant motions will occur on times ranging from picoseconds to microseconds, rather than only the nanoseconds available to thermodynamic integration.…”

Section: Discussionmentioning

confidence: 99%

Conformational dependence of a protein kinase phosphate transfer reaction

Henkelman

LaBute

Tung

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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Atomic motions and energetics for a phosphate transfer reaction catalyzed by the cAMP-dependent protein kinase are calculated by plane-wave density functional theory, starting from structures of proteins crystallized in both the reactant conformation (RC) and the transition-state conformation (TC). In TC, we calculate that the reactants and products are nearly isoenergetic with a 20-kJ/mol barrier, whereas phosphate transfer is unfavorable by 120 kJ/mol in the RC, with an even higher barrier. With the protein in TC, the motions involved in reaction are small, with only P␥ and the catalytic proton moving >0.5 Å. Examination of the structures reveals that in the RC the active site cleft is not completely closed and there is insufficient space for the phosphorylated serine residue in the product state. Together, these observations imply that the phosphate transfer reaction occurs rapidly and reversibly in a particular conformation of the protein, and that the reaction can be gated by changes of a few tenths of an angstrom in the catalytic site.protein dynamics ͉ quantum chemistry ͉ reaction kinetics P rotein kinases regulate many biological processes by transferring a phosphate group from adenosine triphosphate (ATP) to the side chains of particular serine, threonine, or tyrosine residues. The bulky, charged phosphate group alters the conformation and function of the target protein (1, 2). Different kinases recognize different primary sequence motifs surrounding the residue to be phosphorylated, in a highly regulated fashion (3-6). Structural studies have revealed several conformational changes, such as closing of the active-site cleft, the packing of the activation loop, and rotation of the C-helix, which are often implicated in controlling the activity of protein kinases (2). The reasons for such control are clear, but no answer has been provided to such questions as these: ''How closed is closed?'' or ''Is this particular conformation of the activation loop 'good enough' for phosphorylation to occur?'' Quantum chemistry is required to objectively answer these questions.The extent of conformational heterogeneity in a covalent protein reaction was first quantified in a series of experiments monitoring the temperature-dependent rebinding of CO to myoglobin after flash photolysis (7). Agmon and Hopfield created a concise phenomenological model describing this situation, using transition-state theory to describe the vibrational reaction, and a diffusive coordinate that describes the protein conformation and modulates the reaction barrier to the vibrational transition (8, 9). Moving beyond the phenomenological model requires specifying both the conformational heterogeneity and the sensitivity of the reaction barrier to this heterogeneity. Careful structural analysis (10) and quantum chemistry calculations (11) showed that the reaction barrier heterogeneity is indeed a reasonable consequence of observed structural heterogeneity at the myoglobin active site. A reevaluation of a wide variety of myoglobin data also shows ...

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“…2 and 3 also exhibit hydration-shell-coupled motions. Such motions dominate, for instance, the response of photosynthetic reaction center proteins to internal charge separation, where the sensitivity to hydration has been quantified (37)(38)(39). ''Hydration shell'' in this case likely refers to buried water.…”

Section: The ␤-Relaxation In Proteinsmentioning

confidence: 99%

Bulk-solvent and hydration-shell fluctuations, similar to α- and β-fluctuations in glasses, control protein motions and functions

Fenimore

Frauenfelder²,

McMahon³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

506

504

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The concept that proteins exist in numerous different conformations or conformational substates, described by an energy landscape, is now accepted, but the dynamics is incompletely explored. We have previously shown that large-scale protein motions, such as the exit of a ligand from the protein interior, follow the dielectric fluctuations in the bulk solvent. Here, we demonstrate, by using mean-square displacements (msd) from Mö ssbauer and neutron P roteins are the molecules that perform most biological functions, from storage of dioxygen (O 2 ) to enzyme catalysis. A central goal of protein science is to relate structure, dynamics, and function. Although investigations of protein structures and functions are well organized industries, protein dynamics is still in its infancy. Dynamics studies are best performed on proteins whose structures and functions are well known, e.g., myoglobin (Mb), the protein that gives muscles their red color. A hybrid picture of Mb is shown in Fig. 1. The lower part displays a piece of the protein backbone, namely, three ␣-helices. The upper part presents a space-filling view of the protein atoms. The active center, a heme group with a central iron atom, is red. Two cavities are also shown, Xe1 and the heme cavity. The protein is surrounded by the hydration shell, one to two layers of water, and is embedded in the bulk solvent. In Mb's role as an oxygenstorage protein, O 2 enters the protein, stays some time in Xe1, then binds at the heme iron (1). CO follows a similar path through the protein. The structure of Mb shows no permanent channel that leads from the outside to either Xe1 or the heme pocket or from Xe1 to the heme pocket. Thus, structural fluctuations are necessary for function (2).Fluctuations imply that Mb possesses numerous different conformations, called conformational substates (CS) (3). The different CS can be described by an energy landscape (EL) (4), the central concept in the folding (5), dynamics, and function of proteins. The EL is a construct in Ϸ3N dimensions, where N is the number of atoms forming the protein and the hydration shell. A substate is a point in this hyperspace, and structural fluctuations are represented by jumps between points. Initially, we assumed that protein conformations could be organized into a simple, rough EL (1). Experiments showed, however, that there are wells within wells within wells, and an organization of the EL with several tiers of decreasing free-energy barriers ensued (6). The top tier, denoted by CS0, contains a small number of CS with different structures that can have different functions: in A 0 Mb is involved in NO enzymatics; in A 1 it acts as an oxygen-storage system (7). Each of the CS0 substates can assume a very large number of CS1, called statistical substates. They perform the same function but with different rates. Here, we will show that the statistical substates comprise two tiers, CS1␣ and CS1␤. Fluctuations between CS1␣ substates are slaved to the solvent motions and involve sizeable structural changes (8). ...

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Electron Transfer and Protein Dynamics in the Photosynthetic Reaction Center

Cited by 197 publications

References 93 publications

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides

Conformational dependence of a protein kinase phosphate transfer reaction

Bulk-solvent and hydration-shell fluctuations, similar to α- and β-fluctuations in glasses, control protein motions and functions

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Electron Transfer and Protein Dynamics in the Photosynthetic Reaction Center

Cited by 197 publications

References 93 publications

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (QB-•) in Reaction Centers fromRhodobacter sphaeroides

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (QB-•) in Reaction Centers fromRhodobacter sphaeroides

Conformational dependence of a protein kinase phosphate transfer reaction

Bulk-solvent and hydration-shell fluctuations, similar to α- and β-fluctuations in glasses, control protein motions and functions

Contact Info

Product

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ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides

ENDOR Spectroscopy Reveals Light Induced Movement of the H-Bond from Ser-L223 upon Forming the Semiquinone (Q_B^-^•) in Reaction Centers fromRhodobacter sphaeroides