Two-Dimensional Spectroscopy of Chlorophyll a Excited-State Equilibration in Light-Harvesting Complex II

Abstract

ABSTRACT. Excited-state relaxation dynamics and energy-transfer processes in the chlorophyll a (Chl a) manifold of the light-harvesting complex II (LHCII) were examined at physiological temperature using femtosecond two-dimensional electronic spectroscopy (2DES). The experiments were done under conditions free from singlet-singlet annihilation and anisotropic decay. Energy transfer between the different domains of the Chl a manifold was found to proceed on timescales from hundreds of femtoseconds to five picoseconds, before reaching equilibration.No component slower than 10 ps was observed in the spectral equilibration dynamics. We clearly observe the bidirectional (uphill and downhill) energy transfer of the equilibration process between excited states. This bidirectional energy flow, although implicit in the modelling and simulation of the EET processes, has not been observed in any prior transient absorption studies. Furthermore, we identified the spectral forms associated with the different energy transfer lifetimes in the equilibration process. 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 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 3 All photosynthetic organisms rely on light-harvesting antenna systems to maximize the flux of excitation energy at the photochemical reaction centers. Efficient photochemistry relies on the fact that the excitation energy transfer (EET) through the exciton network occurs on a much shorter timescale than the excitation lifetime. Light-harvesting complex II, the most abundant pigmentprotein complex in the biosphere, 1,2 is the major light-harvesting antenna complex in plants and green algae. The relatively rigid protein structure of LHCII 3,4 ensures fine-tuned localization and environment of the noncovalently bound pigment molecules -chlorophyll (Chl) a and b and xanthophylls. The EET dynamics in LHCII has been studied extensively over the past decades using various time-resolved spectroscopic techniques and modelling approaches. Yet, despite the wealth of literature data, there is no complete consensus on the dynamics and pathways of EET, particularly in the equilibration process in the manifold of Chl a exciton states. Upon photoexcitation, due to the narrow spread in energy of the manifold of Chl a exciton states, significant uphill and downhill EET will occur concurrently, leading eventually to a dynamic thermal equilibrium. A wide range of lifetimes for this equilibration process have been reported for LHCII monomers and trimers. At temperatures of 77 K or lower, excitation on the blue side of the Qy band of Chl a is followed by downhill EET with time constants from hundreds of femtoseconds to about 20 ps. 5-8At ...

Measuring Ultrafast Spectral Diffusion and Correlation Dynamics by Two‐Dimensional Electronic Spectroscopy

“…This provides the ability to measure ac orrelation between the excitation and detection frequencies in an ultrafast spectroscopy measurement enablingt he observation of couplings or energy transfers. Various experiments have been carried out using the 2DES technique, ranging from the infrared to the ultraviolet-visible region, studying photosynthetic energy transfer, [3][4][5][6][7][8][9] photochemicalr eactions, [10] and semi-conductor nanoparticle, [11,12] among others.…”

Applications of ultrafast multidimensional electronic spectroscopy to the study of plant light harvesting systems and colloidal quantum dots

“…There has been various applications over a whole range of spectral regions. These include the mid infrared (MIR) region to probe vibrational systems and structural dynamics [173][174][175][176] and visible [7,46,49,133] and ultraviolet (UV) [177] regions for studying natural and artificial light-harvesting systems.…”

“…2D decay-associated spectra of PSI core, resulting from a four-exponential fit of the transient 2D signals from 150 fs to 300 ps with best-fit lifetimes of 0.47 ps, 3.5 ps, 19 ps a non-decaying component. Negative amplitudes (red) represent decay and positive amplitudes -rise of the bleaching signal.pairs of cross/diagonal peaks in the 2D DAS can identify donor-acceptor pairs coupled by reversible (energetically downhill/uphill) EET[133]. The first 2D DAS onFig.…”

“…Furthermore, the slanted ellipsoid shape of the cross peaks shows that multiple states of different energies are engaged in EET. In this respect, exciton equilibration in PSI is reminiscent of spectral diffusion of an inhomogeneously broadened band, which would produce the same characteristic 2D DAS shape[133].The second 2D DAS (3.5 ps lifetime) exhibits a negative peak around λ 3 = 685 nm and a broad positive cross peak at λ 3 = 704 nm. This component can describe well the net downhill EET from the bulk Chls to a pool of Chl a with an absorption band around 700…”

“…We have recently shown that exciton equilibration can be explicitly resolved in the excited-state kinetics of light-harvesting complex II by room-temperature 2DES[133], reducing the uncertainty in ascribing kinetic lifetimes to EET processes (see in Section 3.2 as well). Previously, 2DES was performed on PSI complex from cyanobacteria demonstrating the dynamics of fast EET[134] on the timescale up to several hundred femtoseconds.…”