Ultrafast 2D Spectroscopy of Photosynthetic Light-Harvesting Complexes
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1 Ultrafast 2D Spectroscopy of Photosynthetic Light-Harvesting Complexes PETAR LAMBREV
2 PREAMBLE LASERS IN LIFE SCIENCE LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
3 Preamble LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
4 Preamble Teiz & Zeiger, Plant Physiology, Sinauer Assoc., Inc. LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
5 Preamble It seems likely that in various biological systems energy consuming chemical reactions are coupled to delocalized states of energy Avery, Bay & Szent-Györgyi, 1961 LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
6 Outline 1. The photosynthetic apparatus 2. The plant light-harvesting complex II 3. Principle of 2D electronic spectroscopy 4. 2DES spectroscopy of light-harvesting complex II LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
7 Electron Flow in Photosynthesis LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
8 The Photosynthetic Apparatus Chlorophyll a LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
9 Reaction Centres e Charge separation LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
10 Reaction Centres stroma Q A Q B Pheo e Chl P D1 P D2 thylakoid lumen Photosystem II reaction centre LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
11 Photosystem II Core stroma lumen PDB ID: 3WU2 (Umena et al. 2011) LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
12 PSII-LHCII Supercomplex PDB ID: 5MDX (van Bezouwen et al. 2017) light-harvesting complexes (LHCII) dimeric core complex light-harvesting complexes (LHCII) LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
13 PSII-LHCII Supercomplex light-harvesting complexes (LHCII) dimeric core complex light-harvesting complexes (LHCII) LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
14 Light-Harvesting Complex II PDB ID: 2BHW (Standfuss et al. 2005) trimer top view monomer side view LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
15 ሶ Excitation Energy Transfer S S 0 A* B A B* Förster energy transfer k AB = 9κ2 c 4 8πτ A n 4 R 6 න F A ω σ B ω dω ω 4 Decreases with the sixth power of the distance Is proportional to the overlap of the donor fluorescence spectrum and acceptor absorption spectrum Depends on the mutual orientation of the donor and acceptor κ = μ A μ B 3(R μ A )(R μ B ) Master equation for a system of many pigments: N N p t = k ij p i + k ij p j j i j i LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
16 Molecular Excitons Fassioli et al. (2014) JRS Interface LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
17 Coherent and Incoherent energy transfer LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
18 Measuring Energy Transfer MEASURING ENERGY TRANSFER LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
19 Transient Absorption Spectroscopy Pump pulse excites the system A subsequent probe pulse measures the changes induced by the pump ΔA λ, t = A with pump A without pump 3 rd -order nonlinear response Sample interacts twice with the pump and once with the probe k sig = k 1 k 1 + k 2 = k 2 LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
20 Transient absorption spectra GSB - ground-state bleaching SE - stimulated emission ESA, IA - excited-state absorption, induced absorption M Vengris. Introduction to time-resolved spectroscopy LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
21 2D Coherent Optical Spectroscopy Hamm et al. (2008) Annu Rev Phys Chem 2D optical spectroscopy is the optical analog of 2D NMR Two frequency axes (pump and probe) Negative signals (GS bleaching, emission) and positive signals (ES absorption) Cross peaks (ω pump ω probe ) reflect coupling between oscillators LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
22 2D Electronic Spectroscopy Fassioli et al. (2014) JRS Interface LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
23 Quantum Coherence Energy eigenstates: Solutions to the time-independent Schrödinger equation Hψ r = Eψ(r) States of sharply defined energy: ΔE = E 2 E 2 = 0 Stationary states: Ψ Ψ = ψ e +iet/ħ ψe iet/ħ = ψ ψ Quantum superposition states: Ψ a = c 1 Ψ 1 + c 2 Ψ 2 = = c 1 ψ 1 e ie 1t/ħ + c 2 ψ 2 e ie 2t/ħ Non-stationary Observable values oscillate in time Interference Wave functions of two eigenstates and one superposition state of a harmonic oscillator LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
24 Fourier Transforms መf ξ = න f x e 2πixξ dx The frequency-domain function መf ξ is the Fourier transform of the timedomain function f x LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
25 Pulse Sequence The sample interacts with three pulses: 1. The 1 st pulse creates coherence two states t 1 (coherence time): Oscillations with frequency ω 1 2. The 2 nd pulse may create population, if in phase t 2 (population waiting time, T w ): energy transfer, etc. 3. The 3 rd pulse probes the system t 3 (detection time): emitted photon echo signal oscillating with ω 3 Stimulated echo signal is recorded as S(ω 1, t 2, ω 3 ) LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
26 2DES Experimental Setup Partially collinear pump-probe geometry 2DES LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
27 Transient 2D Electronic Spectroscopy a b ω A ω B Diagonal peaks at the absorption wavelength of each state Cross-peak at (λ 1 = A, λ 3 = B) reflects energy transfer from a to b λ 1 = A donor s Abs wavelength λ 3 = B acceptor s Abs wavelength LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
28 Transient 2D Electronic Spectroscopy a b ω A 2 ps Diagonal peaks at the absorption wavelength of each state Cross-peak at (λ 1 = A, λ 3 = B) reflects energy transfer from a to b ω B λ 1 = A donor s Abs wavelength λ 3 = B acceptor s Abs wavelength LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
29 Coherent Dynamics Exciton coherence: Coherent superposition of eigenstates exhibits oscillatory behavior Cross-peaks in the 2D spectrum oscillate with waiting time The oscillation frequency reflects the energy split between the eigenstates Chenu & Scholes 2015 Annu Rev Phys Chem LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
30 PROBING ENERGY TRANSFER IN LHCII BY 2DES LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
31 Chl b Chl a Energy Transfe Narrowband pump pulses centred at 650 nm excite Chl b states Broadband probe pulses cover all Chl Qy transitions LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
32 2D spectral evolution Chl b excitation Wells KL, Lambrev PH et al. (2014) Phys LASERS Chem IN MEDICINE Chem AND LIFE Phys SCIENCE, 16:11640 SZEGED
33 2D Spectra of LHCII Multistep energy transfer pathways: 650 nm decay of high-energy Chls 680 nm rise of low-energy Chls 665 nm intermediate states LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
34 2D Time Traces A C B D A. Diagonal traces (Chl b): High-energy states decay faster Low-energy states decay slower B. High-energy Chl a Fast rise to a transient maximum Slow (ps) decay Strong coupling with cm -1 Intermediate states C. Mid-energy Chl a Strong coupling with cm -1 Strong dependence on ω 1 D. Low-energy Chl a Multiphasic rise kinetics Not dependent on ω 1 Wells KL, Lambrev PH, Zhengyang Z et al. (2014) Phys Chem Chem Phys Final energy acceptor states LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
35 Global Analysis a b ω A 2 ps ω B S λ 1, λ 3, t = A i λ 1, λ 3 n i=1 e t τ τ lifetimes A i λ 1, λ 3 2D DAS negative peaks population decay positive peaks population rise Wells KL, Lambrev PH et al. (2014) Phys Chem Chem Phys LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
36 2D Decay-Associated Spectra Enriquez MM, Akhtar P et al. (2015) J Chem Phys LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
37 Summary Chl b excitation 65% Chl b Chl a in ps 35% Chl b Chl a in 2 3 ps Intermediate Chl a states ( nm) coupled to low-energy Chl b Different Chl a Chl a ( nm) EET in trimers and aggregates > 3 ps in solubilized trimers 2 3 ps in LHCII aggregates 0.3ps 3ps 667 3ps LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
38 Exciton Relaxation in the Chl a Manifold Akhtar P, Zhang C et al. (2017) J Phys Chem Lett LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
39 Spectral Evolution λ 1 = 665 nm λ 1 = 685 nm LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
40 2D DAS of LHCII trimers LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
41 Simulated 2D Spectra LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
42 Energy Transfer between Chl a Domains LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
43 Thank you! LASERS IN MEDICINE AND LIFE SCIENCE, SZEGED
P. Lambrev October 10, 2018
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