Two-dimensional spectroscopy of electronic couplings in photosynthesis

Abstract

Time-resolved optical spectroscopy is widely used to study vibrational and electronic dynamics by monitoring transient changes in excited state populations on a femtosecond timescale. Yet the fundamental cause of electronic and vibrational dynamics--the coupling between the different energy levels involved--is usually inferred only indirectly. Two-dimensional femtosecond infrared spectroscopy based on the heterodyne detection of three-pulse photon echoes has recently allowed the direct mapping of vibrational couplings, yielding transient structural information. Here we extend the approach to the visible range and directly measure electronic couplings in a molecular complex, the Fenna-Matthews-Olson photosynthetic light-harvesting protein. As in all photosynthetic systems, the conversion of light into chemical energy is driven by electronic couplings that ensure the efficient transport of energy from light-capturing antenna pigments to the reaction centre. We monitor this process as a function of time and frequency and show that excitation energy does not simply cascade stepwise down the energy ladder. We find instead distinct energy transport pathways that depend sensitively on the detailed spatial properties of the delocalized excited-state wavefunctions of the whole pigment-protein complex.

Dynamics of a Multimode System Coupled to Multiple Heat Baths Probed by Two-Dimensional Infrared Spectroscopy

“…For those systems, 2D electronic spectra provide detailed information on the electronic couplings among chromophores and on the excited energy and coherence transfer. [61][62][63][64][65] We leave them for future studies. Figure 3.…”

Two-Dimensional Spectroscopy of Extended Molecular Systems: Applications to Energy Transport and Relaxation in an α-Helix

“…In particular, the analogues of the NOESY variant of 2DNMR allow for the study of dynamics, because they involve a waiting time t 2 that may be controlled at the femtosecond time scales, thus allowing one to take snapshots of a system while it evolves. 2,3 Examples of systems that have been studied using 2DIR or 2Dvis spectroscopies with nonzero waiting times include relatively simple few-level systems, such as the coupled amide I and amide II vibrations in N-methylacetamide (NMA) 4 and vibrations in other small organic molecules, 5 as well as extended systems with a multitude of levels, such as the amide I band in polypeptides or proteins, 6,7 the excitonic transitions in the photosynthetic Fenna-Matthew-Olsen complex, 8 and the excitonic transitions in double-wall molecular nanotubes. 9 In the simplest situation, with only two interacting vibrational or electronic states of interest, it is rather straightforward to obtain information about their coupled dynamics from the waiting time dependence of the 2D spectrum.…”

The molecular origin of high DNA-repair efficiency by photolyase

“…P hotochemical machines in nature are powered by sunlight to execute important biological functions such as photosynthesis for light energy conversion to chemical energy and photosensory function for signal transduction [1][2][3][4][5][6] . To reach high biological efficiency, the initial photoinduced dynamics are usually ultrafast to quickly funnel excitation energy into the functional coordinate(s) and avoid futile energy dissipation into the environment [2][3][4] .…”

“…To reach high biological efficiency, the initial photoinduced dynamics are usually ultrafast to quickly funnel excitation energy into the functional coordinate(s) and avoid futile energy dissipation into the environment [2][3][4] . In addition to photosynthesis and photosignalling, blue light energy is used as a co-substrate for repairing DNA damage by photolyase with high quantum yield 7,8 .…”