Breaking the Red Limit: Efficient Trapping of Long-Wavelength Excitations in Chlorophyll-f-Containing Photosystem I

Photosystem I (PSI) converts photons into electrons with a nearly 100% quantum efficiency. Its minimal energy requirement for photochemistry corresponds to a 700-nm photon, representing the well-known “red limit” of oxygenic photosynthesis. Recently, some cyanobacteria containing the red-shifted pigment chlorophyll f have been shown to harvest photons up to 800 nm. To investigate the mechanism responsible for converting such low-energy photons, we applied steady-state and time-resolved spectroscopies to the chlorophyll-f-containing PSI and chlorophyll-a-only PSI of various cyanobacterial strains. Chlorophyll-f-containing PSI displays a less optimal energetic connectivity between its pigments. Nonetheless, it consistently traps long-wavelength excitations with a surprisingly high efficiency, which can only be achieved by lowering the energy required for photochemistry, i.e., by “breaking the red limit”. We propose that charge separation occurs via a low-energy charge-transfer state to reconcile this finding with the available structural data excluding the involvement of chlorophyll f in photochemistry. [Display omitted] •Chlorophyll f insertion reduces energetic connectivity between Photosystem I pigments•Chlorophyll f excitations are efficiently trapped via a low-energy state•Location and function of chlorophyll f within the complex are discussed•Chl-f-containing photosystem I of various cyanobacteria share the same properties Because of its energetic requirements, oxygenic photosynthesis employs a particular chlorophyll, chlorophyll a, which only absorbs visible light up to 700 nm. This spectral restriction can be particularly limiting under the shade of a dense plant canopy, where the available light is highly enriched in far-red photons (700–800 nm). Therefore, a promising approach for increasing biomass yields is to push light-harvesting capacity beyond the natural spectral limits by introducing pigments absorbing at longer wavelengths than chlorophyll a. Interestingly, a group of cyanobacteria is capable of harvesting far-red light up to 800 nm by integrating the red-shifted chlorophyll f in their photosystems. Here, we clarify the molecular mechanisms allowing chlorophyll-f-containing photosystem I to collect and process such low-energy photons with surprisingly high efficiency, thus providing a starting point for optimizing the photosynthetic units of other organisms. Although oxygenic photosynthesis typically uses chlorophyll a and is powered by vi