Vibronic coherence in oxygenic photosynthesis

Abstract

Photosynthesis powers life on our planet. The basic photosynthetic architecture consists of antenna complexes that harvest solar energy and reaction centres that convert the energy into stable separated charge. In oxygenic photosynthesis, the initial charge separation occurs in the photosystem II reaction centre, the only known natural enzyme that uses solar energy to split water. Both energy transfer and charge separation in photosynthesis are rapid events with high quantum efficiencies. In recent nonlinear spectroscopic experiments, long-lived coherences have been observed in photosynthetic antenna complexes, and theoretical work suggests that they reflect underlying electronic-vibrational resonances, which may play a functional role in enhancing energy transfer. Here, we report the observation of coherent dynamics persisting on a picosecond timescale at 77 K in the photosystem II reaction centre using two-dimensional electronic spectroscopy. Supporting simulations suggest that the coherences are of a mixed electronic-vibrational (vibronic) nature and may enhance the rate of charge separation in oxygenic photosynthesis.

Coherence and population dynamics of chlorophyll excitations in FCP complex: Two-dimensional spectroscopy study

“…In the 2D ES spectra of FCP we would expect coherences of various origins and amplitudes to appear: ground state vibrational coherences of Chl a, Chl c and Fx, excited state vibronic coherences of the same frequencies, mixed coherences of shifted or combinational frequencies 16,45 and electronic coherences due to excitonic coupling of chlorophylls. Such distinction between the coherences of different origin is conveniently observed in the Fourier amplitude maps.…”

“…The energy gap of 715 cm −1 is close to the strongest vibrational Chl a mode of 745 cm −1 , thus allowing for electronic-vibrational resonance [55][56][57] . Recently, specific vibrational modes were suggested to speed up the initial charge transfer step in the photosystem II (PS II) reaction center 16,17 . Finally, this does not contradict our previous suggestion that Chl c is coherently coupled to Chl a 12 , however, the coherent mechanism may be far more complicated and calls for future studies.…”

“…The first and the most recognized results of 2D ES demonstrating complex behavior of the excitation evolution were delivered for the photosynthetic FennaMatthews-Olson (FMO) complex from purple bacteria 13 . Since then, 2D ES has been successfully applied for studies of a number of different systems; 2D ES es-sentially helped to establish or update existing kinetic schemes of light-harvesting antennae and reaction centers of plants [14][15][16][17] and bacteria [18][19][20] . The 2D ES was also performed on the whole photosystem I complex demonstrating signatures of fast energy transfer 21 .…”

Determining the static electronic and vibrational energy correlations via two-dimensional electronic-vibrational spectroscopy

“…Recently, an increasing number of experimental studies suggested the possibility of active engagement of molecular vibrational excited states in charge separation [1][2][3] . In a pump-push experiment on organic photo-voltaic cells, Bakulin et.…”

Energy transfer in structured and unstructured environments: Master equations beyond the Born-Markov approximations

“…[16][17][18][19] In addition to the (often low frequency) continuum, the environmental spectral densities of pigment-protein complexes are generally structured; that is, there are specific underdamped vibrational modes of the environment that couple strongly to the excitonic degrees of freedom. There is now increasing evidence to suggest that these underdamped modes are an important contributing factor to the long-lived coherences observed in photosynthetic systems, [20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] as well as links between the quantum mechanical nature of these vibrational modes and enhanced transfer rates. 25,37,39,40 A multitude of powerful computational methods have been developed to deal with the difficulties faced in modelling strongly dissipative quantum systems.…”