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The recently discovered, chlorophyll-f-containing, far-red photosystem II (FR-PSII) supports far-red light photosynthesis. Participation and kinetics of spectrally shifted far-red pigments are directly observable and separated from that of bulk chlorophyll-a. We present an ultrafast transient absorption study of FR-PSII, investigating energy transfer and charge separation processes. Results show a rapid subpicosecond energy transfer from chlorophyll-a to the long-wavelength chlorophylls-f/d. The data demonstrate the decay of an ∼720-nm negative feature on the picosecond-to-nanosecond timescales, coinciding with charge separation, secondary electron transfer, and stimulated emission decay. An ∼675-nm bleach attributed to the loss of chl-a absorption due to the formation of a cation radical, PD1+•, is only fully developed in the nanosecond spectra, indicating an unusually delayed formation. A major spectral feature on the nanosecond timescale at 725 nm is attributed to an electrochromic blue shift of a FR-chlorophyll among the reaction center pigments. These time-resolved observations provide direct experimental support for the model of Nürnberg et al. [D. J. Nürnberg et al., Science 360, 1210–1213 (2018)], in which the primary electron donor is a FR-chlorophyll and the secondary donor is chlorophyll-a (PD1 of the central chlorophyll pair). Efficient charge separation also occurs using selective excitation of long-wavelength chlorophylls-f/d, and the localization of the excited state on P720* points to a smaller (entropic) energy loss compared to conventional PSII, where the excited state is shared over all of the chlorin pigments. This has important repercussions on understanding the overall energetics of excitation energy transfer and charge separation reactions in FR-PSII.

Significance The E m of Q A / Q A − • is the reference pegging the thermodynamics of Photosystem II (PSII) to an absolute value. This work resolves a long-standing discrepancy in the literature, removing this ambiguity at the heart of PSII bioenergetics. The discrepancy in the literature reflects the loss of bicarbonate in some titrations. This surprising finding shows that bicarbonate binding controls the E m of Q A / Q A − • , and thus the redox state of Q A influences the binding of bicarbonate. This process constitutes a previously unrecognized regulation of PSII: Q A − • triggers bicarbonate release, slowing electron transfer and tuning the potential of Q A to protect PSII against photodamage. This work provides an explanation for the existence of bicarbonate in PSII, a mystery for more than half a century.