Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes

Abstract

Energy transfer in photosynthesis occurs as electronic excitations of coupled chromophores interact with their environment. The microscopic nature of these motions can enable novel energy-transfer mechanisms if the motions are not random. This study reveals synchronized and correlated fluctuations of the states within a photosynthetic pigment-protein complex, which explains prior observations of long-lived quantum coherence. SUMMARYEarly reports of long-lived quantum beating signals in photosynthetic pigmentprotein complexes were interpreted to suggest that electronic coherence benefits from protection by the protein, but many subsequent studies have suggested instead that vibrational or vibronic contributions are responsible for the observed signals. Here, we devised two 2D-spectroscopy methods to observe how each exciton is perturbed by its nuclear environment in a photosynthetic complex. The first approach simultaneously monitors each exciton's energy fluctuations over time to obtain its time-dependent electronic-nuclear interactions. The second method isolates evidence of coupled interexcitonic environmental motions. The techniques are validated with Nile Blue A and subsequently used on the Fenna-Matthews-Olson (FMO) complex. The FMO data reveal that each exciton experiences nearly identical spectral motion after excitation and that spectral motion of one excited exciton induces similar motion on unpopulated neighboring excitonic states. These synchronized and correlated spectral dynamics prolong coherences in the FMO complex after femtosecond excitation.

Quantum biology revisited

“…This correlation has not been included in the theoretical considerations above. A number of studies have advocated such "environmental protection of excitonic coherence" as the source of long-lived oscillations in 2D spectra (59)(60)(61). However, no quantum mechanics/ molecular mechanics based dynamic studies of the FMO protein could identify correlations in site energy fluctuations (22,25).…”

Vibronic mixing enables ultrafast energy flow in light-harvesting complex II

“…At the same time, long-lived oscillatory features were observed, initially in the FMO complex 13 and later in LHCII 9 . Since then, the origin of these oscillations has been extensively debated [14][15][16][17][18][19][20][21][22][23][24][25][26] . Beyond this debate lies an even more challenging question-how does the observation of these beats spectroscopically connect to the mechanistic function of natural light-harvesting?…”

Collective Excitations in α-helical Protein Structures Interacting with the Water Environment

“…Different types of the collective modes are reported to be excited in protein molecules, i.e. normal vibration modes (Acbas et al, 2014;Turton et al, 2014), sound waves (phonons) (Liu et al, 2008), and coherent vibrational states (Del Giudice et al, 1986;Rolczynski et al, 2018) which are observed on a timescale from picosecond to nanosecond. Vital cellular processes are suggested to link to the excitation of the long-lived collective degreases of freedom in macromolecules which are characterised by a weak coupling to the other ones and related to the substantially non-equilibrium processes in proteins (Mohseni et al, 2014).…”