Structures of photosynthetic pigment-protein
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1 Structures of photosynthetic pigment-protein protein complexes and probing electrostatic field inside them by Stark spectroscopy Hideki Hashimoto, 1 Ritsuko Fujii, 1 Satoru Suzuki, 1 Katsunori Nakagawa, Mamoru Nango, Aleksander W. Roszak, 3 Alastair T. Gardiner, 3 Richard J. Cogdell, 3 Shin-ichi Adachi, 4,6 and Shin-ya Koshihara 5,6 1 Department of Physics, Osaka City University, Japan Department of Materials Engineering, Nagoya Institute of Technology, Japan 3 Institute of Biomedical and Life Sciences, University of Glasgow, Scotland, UK 4 Institute of Materials Structure Science, KEK, Japan 5 Department of Materials Science, Tokyo Institute of Technology, Japan 6 Non-equilibrium Dynamics Project, ERATO/JST, Japan ; hassy@sci.osaka-cu.ac.jp
2 Contents A comparative look at the structural requirements for photosynthetic light-harvesting Structural study of the RC of purple photosynthetic bacteria Stark spectroscopy on the native and reconstituted pigment-protein complexes of purple photosynthetic bacteria
3
4 The structure of all photosynthetic reaction centres is strongly conserved. This is because the structural constraints on electron transfer are very strict. A comparison of the structures of photosynthetic light-harvesting complexes shows that they form a very heterogeneous group. Why is this?
5 LHCII from spinach
6 Peridinin- Chlorophyll a complex
7 LH complexes
8 The physics of energy transfer is rather tolerant. This means that there are many structural solutions to the problem of building an efficient light-harvesting complex.
9 Absorption spectrum of the chromatophores of Rb. sphaeroides LH B85 Absorbance B Car B8 B875 (LH1) Q x Q y Wavelength / nm
10 Photosynthetic system of purple bacteria in the intracytoplasmic membrane Light Periplasm H + LH LH1 e - e - Cytochrome b/c 1 H + Cyt c B85 B88 B8 RC Q B Q Q Q Q Q Q Q e - ADP + P i ATP H + ATP synthase Cytoplasm Q B Fe H + Q A System of pigments in RC
11
12 Contents A comparative look at the structural requirements for photosynthetic light-harvesting Structural study of the RC of purple photosynthetic bacteria Stark spectroscopy on the native and reconstituted pigment-protein complexes of purple photosynthetic bacteria
13 Structure of the photosynthetic RC M-subunit L-subunit P Car B B B A H A H B Q B Fe Q A H-subunit Shown above is the structure of RC from Rhodobacter sphaeroides, Roszak, Hashimoto, Cogdell, and Frank, et al. (4) Structure, 1, 765.
14 Electron transfer in the RC Bchla Primary donor P M P hν P* P + L Accessory Bchla 3ps Pheophytin Spheroidene Ubiquinone-1 15µs ps Q B Fe + Q A
15 Our high-resolution (1.95 Å) X-ray crystal structure analysis of the wild-type RC from Rba. sphaeroides strain.4.1
16 Electron densities of the surfactant molecules surrounding the RC
17 Solvent molecules surrounding the RC
18 Contents A comparative look at the structural requirements for photosynthetic light-harvesting Structural study of the RC of purple photosynthetic bacteria Stark spectroscopy on the native and reconstituted pigment-protein complexes of purple photosynthetic bacteria
19 Research Background Osaka City University
20 Research Background Osaka City University Great success of X-ray crystallography on pigment-protein complexes of purple photosynthetic bacteria Ultra-fast laser spectroscopy to understand each step of energy and electron transfer
21 Research Background Osaka City University It is important to understand the exact mechanisms of electrostatic interaction between pigments and their surrounding proteins in order to clarify the true functional mechanisms of the pigments in photosynthesis
22 Characteristics of electroabsorption (Stark effect) spectroscopy Pigments in pigment-protein complexes are under the influence of internal electric field produced by the electrostatic potential of apoprotein Electroabsorption spectroscopy is one of the most promising methods to probe the pigment-protein interaction modulated by the external electric field
23 Optical absorption spectra under the influence of external or internal electric field Intensity change Spectral shift Broadening & Shrinkage A A A Absorbance Absorbance Absorbance Photon energy Photon energy Photon energy
24 Liptay equation A( ν ) = A( ν, E int ) A( ν,) d( A ν ) = ( DA( ν,) + Fν + hdν d ( A ν ) Hν ) E h dν int R( χ, ζ ) A B D = +, A µ F = + α, M M M H = µ R( χ, ζ) = M( F hν m int ( F int (5 + (3cos ) = M + AE ) = hν m int ζ 1)(3cos + E int () µe BE int int 1 E χ 1)) /15 int αe int Stark effect
25 Experimental setup for electroabsorption spectroscopy Monochromater Pre-amplifier Sample cell f Photo-diode Bipolar power amplifier f AC DC Dual-phase Lock-in amp PC
26 Contents of this presentation 1. Local electrostatic field induced by carotenoid in the reaction centre of purple photosynthetic bacteria [ J. Phys. Chem. B 19 (5) ]. Stark spectroscopy on the LH complex from Rhodobacter sphaeroides strain G1C; frequency and temperature dependence [J. Phys. Chem. B 18 (4) ]
27 Contents of this presentation Local electrostatic field induced by carotenoid in the reaction centre of purple photosynthetic bacteria [ J. Phys. Chem. B 19 (5) ]
28 Objective Evaluation of electrostatic effect of Car on Bchls (especially P) in RC Electroabsorption (EA) spectra of two reaction centres were recorded One is prepared from Rb. sphaeroides strain R6.1 (R6.1-RC), which lacks carotenoid R6.1-RC
29 Objective Evaluation of electrostatic effect of Car on Bchls (especially P) in RC Electroabsorption (EA) spectra of two reaction centres were recorded The other one is a reconstituted RC (R6.1 -RC+ Car) which was prepared by re-incorporating synthetic Car (3,4- dihydrospheroidene) into R6.1-RC R6.1-RC+Car
30 Objective Evaluation of electrostatic effect of Car on Bchls (especially P) in RC The electrostatic effect of Car on P was evaluated from the difference of these two spectra
31 Gatekeeper (Phe M16) and locking (Trp M75) amino acid residues in the site of RC where Car is re-incorporated Trp M75 Phe M16 A.W. Roszak, K. McKendrick, A.T. Gardiner, I.A. Mitchell, N.W. Isaacs, R.J. Cogdell, H. Hashimoto, and H.A. Frank, Structure, 1, 4, 765.
32 Influence of static-electric field on the excited state of Bchls caused by the presence of Car Electrostatic field F around Bchls in RC F = F + F + a p F c F a : applied electric field F p : pocket field F c : static-electric field due to Car
33 Absorption change due to applied electric field Absorption change ( A) due to applied electric field can be written as, A = 1 3 DA F d A ν + dν 1 6 d A ν F µ * dν a ( X + µ ) 1 eg eg D F = Tr[ α] + µ * Tr[ α] = Y µ eg µ µ X eg µ * = µ + α F + α F int p c
34 Influence of Car on Bchl Change of µ value by static-electric field due to the presence of Car µ = α c F c This change is expected to be observed by EA spectroscopy The contribution of µ is detected as the second-order derivative waveform of absorption spectra in EA spectra. Therefore, the second derivative waveform should be observed in the difference EA spectra between R6.1-RC and R6.1-RC+Car.
35 Electroabsorption spectra of RC s from Rb. sphaeroides R6.1 at 79 K In-phase Quadrature-phase Normalized absorbance 1 5 B H P (a) Rb. sphaeroides R6.1 at 79 K Normalized absorbance 1 5 B H P (d) Rb. sphaeroides R6.1 at 79 K Normalized A in [ 1 6 ] (b) Rb. sphaeroides R6.1+ Car (c) (a) (b) Normalized A quad [ 1 6 ] (e) Rb. sphaeroides R6.1+ Car (f) (d) (e) Wave number [cm 1 ] Wave number [cm Physics of Biological Materials 1 ] Lab.
36 Electroabsorption spectra of RC s from Rb. sphaeroides R6.1 at 93 K In-phase Quadrature-phase Normalized absorbance B P H (a) Rb. sphaeroides R6.1 at 93 K Normalized absorbance 1 5 B P H (d) Rb. sphaeroides R6.1 at 93 K Normalized A in [ 1 6 ] (b) Rb. sphaeroides R6.1+ Car (c) (a) (b) Normalized A quad [ 1 6 ] (e) Rb. sphaeroides R6.1+ Car (f) (d) (e) Wave number [cm 1 ] Wave number [cm Physics of Biological Materials 1 ] Lab.
37 79 K Nonlinear optical parameters of P band P band D [1-18 (m/f L V) ] Tr[ α] [Å 3 /f L ] µ [D/f L ] R6.1-RC (..3) R6.1+Car-RC (.4.8) K R6.1-RC (1.7.1) R6.1+Car-RC (1.7.4) F a = f L F ext F ext is externally applied electric field. f L is a local field correction factor. Even if the experimental errors are taken into account, the difference of µ between R6.1-RC and R6.1- RC+Car at 93 K is estimated to be ~1. [D].
38 Nonlinear optical parameters of B band 79 K 93 K B band D [1-18 (m/f L V) ] Tr[ α] [Å 3 /f L ] µ [D/f L ] R6.1-RC.9. -(1..4) R6.1+Car-RC (1.1.) 1.9. R6.1-RC ( ) R6.1+Car-RC (5.8.4) µ of B band is different between R6.1-RC and R6.1-RC+Car at 93 K.
39 Nonlinear optical parameters of H band 79 K 93 K H band D [1-18 (m/f L V) ] Tr[ α] [Å 3 /f L ] µ [D/f L ] R6.1-RC.4. -(8.4 7.) R6.1+Car-RC.4.1 -(.9.) R6.1-RC.8. (9.5.3) R6.1+Car-RC.8.3 (1. 4.) No significant difference is observed between R6.1-RC and R6.1+Car-RC in the nonlinear optical parameters of H band
40 Estimation of static-electric field induced by the presence of carotenoid µ c = α Fc 1.[ D / f L] Fc [V cm] f L =. b Reported localized field around P is ~1 1 6 [V/cm]. a The presence of Car causes ~1 % change of the electrostatic environment around P. According to our results of X-ray crystallography of RC, c carotenoid binding pocket becomes smaller when Car is absent. This may cause some rearrangements of amino acid residues around P. As a consequence, the above ~1 % change should be occurred. [a] T.R. Middendorf et al., BBA, 1143, 1993, 3. [b] M. Loche et. al., PNAS, 84, 1987, [c] A.W. Roszak et al., Structure, 1, 4, 765.
41 Conclusions on RC Carotenoid bound to the RC was found to affect on the electrostatic environment around P and B (B B ). The static electric field on P due to the presence of carotenoid was estimated to be ~ [V/cm]. It corresponds to as high as 1% of the local electric field around P. Carotenoid could be one of the important factors that regulate the function of P (vice versa).
42 Contents of this presentation 1. Local electrostatic field induced by carotenoid in the reaction centre of purple photosynthetic bacteria [ J. Phys. Chem. B 19 (5) ]. Stark spectroscopy on the LH complex from Rhodobacter sphaeroides strain G1C; frequency and temperature dependence [J. Phys. Chem. B 18 (4) ]
43 Contents of this presentation Stark spectroscopy on the LH complex from Rhodobacter sphaeroides strain G1C; frequency and temperature dependence [J. Phys. Chem. B 18 (4) ]
44 How can we evaluate electrostatic interaction between pigments and apoproteins? Most previous reports on the use of Stark spectroscopy to study photosynthetic pigment-protein complexes have only used in-phase signals More detailed information on dynamic electrostatic interactions with the environment can be obtained from out-ofphase (quadrature-phase) signal
45 How can we evaluate electrostatic interaction between pigments and apoproteins? By studying the frequency and temperature dependence of the quadrature-phase signals the nature of the pigment-protein interaction can be investigated!
46 Absorption spectra of the LH complex from Rb. sphaeroides G1C (a) (b) Normalized absorbance Normalized absorbance 1 1 in buffer solution in PVA matrix Wavelength [nm]
47 Electro-absorption spectra of the LH complex from Rb. sphaeroides G1C (a) (b) Normalized Absorbance A in [ 1 5 ] 1 1 in phase (c) A quad [ 1 6 ] quadrature phase Wavenumber [cm 1 ]
48 Theoretical model to generate the phase-retarded signals Α = ( µ * E) A 1 E : α : E A 1 ( µ * E) h + ν h + ν µ * = µ + α : mol E pocket h A ν E pocket ( x) = E ( ) + C x pocket µ is dipole-moment change upon photoexcitation α is polarizability change upon photoexcitation
49 d x dt Dependence of the phase-retarded signals on the modulation frequency of the applied electric field dx = γ dt ω x + q E m ( ) ) ω ω + γ ω E( t) = f E sin( ωt) q f ( ) L Eext x t = sin( ωt 1/ m L ext + φ ) p tanφ p = γω ω ω
50 Absorption change modulated with ω frequency ( ) ( ) cos 6 1 cos 3 x ext L * ext L t E f A h A h t E f A h C A ω ν ν ν µ ν ν ν α φ ω ν ν ν α ω + + =
51 In-phase signals detected by a dual-phase lock-in amplifier ( ) ( ) 6 1 cos x 6 1 ext L * in ext L * in E f h A h A F E f h A A h α C h A + = + + = ν ν ν µ ν ν ν ν ν ν µ ν ν ν φ α ( ) ( ) ( ) + + = + = n 1 cos x 1 ω γ ω ω ω ω α φ α m qc C F i
52 Quadrature-phase signals detected by a dual-phase lock-in amplifier ( ) 6 1 sin x 6 1 ext L quad ext L quad E f h A F E f h A α C A = = ν ν ν ν ν ν φ ( ) quad sin x ω γ ω ω γω α φ α + = = m qc C F
53 Temperature dependence of in-phase and quadrature-phase EA spectra (a) A in Normalized 1 93K 1 7K 1 K 79K Wavenumber [cm 1 ] (b) A quad Normalized K 7K K 79K Wavenumber [cm Physics of Biological 1 ] Materials Lab.
54 Temperature dependence of F quad / F in value + + = RT H C q m F F r exp 1 ] ) [( τ ω ω ω γ ω ω ω γ 1 in quad H is the activation energy that characterizes the relaxation factor γ
55 Temperature dependence of F quad / F in value F quad / F in.6.4. H ~ 1 kj / mol 1 3 Temperature [K] Quite a number of molecular motions can be plausible candidates that generate the relaxation factor, γ. For example, local mode relaxation, crankshaft and kink motion, rotation of methyl group, side chain motion, local intermolecular rearrangements etc.
56 Temperature dependence of F quad / F in value F quad / F in.6.4. H ~ 1 kj / mol 1 3 Temperature [K] Inspection of X-ray crystal structure of the LH complex from Rps. acidophila strain 15, suggests that a plausible candidate for the physical origin of γ could be either a local twisting motion of the apoprotein main chain, or rotational motion of apoprotein side chains
57 Frequency dependence of F quad value F quad ( f ) = qc α m ( ) ω 4π f + 4π γ f πγf ω = πf
58 Dependence of the phase-retarded signals on the modulation frequency F quad ( f ) / F quad (5) Frequency [ f ] sec m sec sec n sec p sec f sec ω ~ 11 khz Rotation of an aromatic side chainofanaminoacidresidue inside a protein Deformation vibration Stretching vibration
59 The X-ray crystal structure of the LH complex from Rps. acidophila strain 15 clearly shows that the Mg + ions at the centre of the B85 bacteriochlorin rings are liganded to histidine side chains. These histidine residues are prime candidates for the strong electrostatic interaction suggested by the presence of the phase-retarded signals. However, the resonance frequency of 11 khz looks too low for a normal mode reflecting the Mg-His interaction (~1 THz). LH subunit of Rps. acidophila 15
60 The relevant normal mode could be an overall, coupled mode reflecting the total environment of pigment-protein interaction LH subunit of Rps. acidophila 15
61 Conclusions on LH Electroabsorption (Stark effect) signals due to electrostatic interactions between the B85 pigments and surrounding apoproteins were detected as a phase-retarded signal using dual-phase lock-in detection The Arrhenius type activation energy (H = 1 kj/mol) was determined from the temperature dependence of the phaseretarded signals. The resonance frequency (ω = 11 khz) was determined from their frequency dependence. The calculated thermodynamic and kinetic parameters can be accounted for by assuming a strong electrostatic interaction of the B85 pigments with the dynamic environment provided by the apoproteins.
62 Thank you for your attention!
It s really this simple.
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