The Energy Transfer Yield between Carotenoids and Chlorophylls in Peridinin Chlorophyll a Protein Is Robust against Mutations

Abstract

The energy transfer (ET) from carotenoids (Cars) to chlorophylls (Chls) in photosynthetic complexes occurs with almost unitary efficiency thanks to the synergistic action of multiple finely tuned channels whose photophysics and dynamics are not fully elucidated yet. We investigated the energy flow from the Car peridinin (Per) to Chl a in the peridinin chlorophyll a protein (PCP) from marine algae Amphidinium carterae by using two-dimensional electronic spectroscopy (2DES) with a 10 fs temporal resolution. Recently debated hypotheses regarding the S2-to-S1 relaxation of the Car via a conical intersection and the involvement of possible intermediate states in the ET were examined. The comparison with an N89L mutant carrying the Per donor in a lower-polarity environment helped us unveil relevant details on the mechanisms through which excitation was transferred: the ET yield was conserved even when a mutation perturbed the optimization of the system thanks to the coexistence of multiple channels exploited during the process.

Intramolecular charge-transfer enhances energy transfer efficiency in carotenoid-reconstituted light-harvesting 1 complex of purple photosynthetic bacteria

“…However, the most striking finding in this study is that the S 1 /ICT state becomes the major EET channel in Reβapo. This idea is supported by the recent publication by Tumbarello et al 44 .…”

Two-Dimensional Electronic Spectroscopy Characterization of Fucoxanthin–Chlorophyll Protein Reveals Excitonic Carotenoid–Chlorophyll Interactions

“…The decay of these ultrafast signals, damped in a time scale comparable with the laser pulse duration, allows for the emergence of the two main signals that dominate the maps for delay times > 50 fs (Figures b). In the longer time scale, indeed, the 2DES maps show a positive diagonal peak with an excitation frequency of ∼16300 cm –1 , mainly related to the Stimulated Emission (SE) and the Ground State Bleaching (GSB) of the Chls a bands, , and a broad negative signal with an excitation frequency (x-coordinate) of ∼17700 cm –1 , corresponding to the typical Excited State Absorption (ESA) signals of the carotenoids. − The amplitude distribution of this ESA signal closely resembles what was previously found for isolated Fx molecules in a methanol solution (Figure S4). The ESA signal has two main maxima, characterized by different y-coordinates in the 2D maps: 16600 and 17500 cm –1 .…”

“…The frequencies identified agree with the well-known vibrational modes of carotenoids (at about 1200, 1280, and 1580 cm –1 ). , Interestingly, the Fx vibrational frequencies do not only affect the ESA band explicitly attributed to dynamics within the Fx, but they also strongly contribute at positions where Chl a and Chl c signals are typically identified, as shown in Figure . These beatings appear at well-defined specific coordinates (see SI, Figure S6), which do not follow the conventional pattern expected for vibrational modes according to the displaced harmonic oscillator model, suggesting the presence of more complex mechanisms at play. , …”

“…These beatings appear at well-defined specific coordinates (see SI, Figure S6), which do not follow the conventional pattern expected for vibrational modes according to the displaced harmonic oscillator model, suggesting the presence of more complex mechanisms at play. 56,66 While a clear attribution has not been proposed yet, the finding that the vibrational oscillation of Fx is delocalized throughout the 2D map could imply that the nuclear degrees of freedom of Fx play a functional role in the redistribution of the energy between chromophores. This interpretation, although very suggestive, remains a hypothesis, and further targeted experiments are needed to confirm it.…”

Ultrafast carotenoid-chlorophyll interactions in fucoxanthin-chlorophyll protein (FCP)

“…This is a well-known feature corresponding to the excited state absorption of the S1 and ICT states of Fx (upper and lower lobe of the band) that dominates the dynamics for t2 > 50 fs. [37][38][39] Figure 3. 2DES maps of FCP at selected values of population time t2; the colored dotted lines in the map at 7.5 fs pinpoint the spectral position of the main bands appearing also in the linear spectrum as highlighted in the upper inset.…”