Plants, algae, and cyanobacteria sustain life on Earth by using sunlight energy to produce oxygen and biomass via oxygenic photosynthesis. It involves water splitting and carbon fixation using the protein complexes photosystem II (PSII) and photosystem I (PSI), respectively. Despite tremendous advances in the field, the dynamics and mechanisms of the underlying processes are not fully understood yet. Ultrafast spectroscopy methods have been particularly versatile in uncovering a lot of detail about these processes; however, the spectral overlap arising from identical pigments has always been a complication. An opportunity to overcome that came along with the recent discovery of red-shifted chlorophyll f (chl-f).
In this work, energy and electron transfer processes of chl-f-containing PSII and PSI from far-red light (FRL)-grown Chrooccidiopsis thermalis PCC 7203 were studied using ultrafast visible and infrared spectroscopy, respectively, and comparisons with standard white light-grown photosystems were made. Sub-picosecond energy transfer from antenna chlorophyll a (chl-a) to far-red chlorophylls (chl-f/chl-d) was revealed in FRL-PSII with excitation being highly localised. The data supported a primary donor role of a far-red chlorophyll and a secondary donor role of chl-a at PD1 position, with an unprecedentedly delayed formation of PD1+•.
In FRL-PSI, a complete energy transfer from chl-a to chl-f within 1 ps was observed. Spectral evolution supported a primary radical pair assignment to A-1+•A0-• with A-1 being a chl-f. Shifts in carbonyl bands corresponding to P700+•/P700 and A1-•/A1 indicated dielectric differences in FRL-PSI environment.
Vibrational properties of chl-f and chl-a in the ground and excited states were studied using density functional theory at B3LYP/6-31G(d) and CAMB3LYP/6-31G(d) levels, with particular interest in carbonyl modes experimentally shown to significantly downshift upon excitation. These downshifts were underestimated by both methods and the calculated Franck-Condon and Herzberg-Teller vibrational progressions demonstrated inaccuracies in the prediction of high-frequency mode displacements.