Excitation Energy Transfer between Higher Excited States of Photosynthetic Pigments: 1. Carotenoids Intercept and Remove B Band Excitations.

Chlorophylls (Chls) are known for fast, subpicosecond internal conversion (IC) from ultraviolet/blue-absorbing ("B" or "Soret" states) to the energetically lower, red light-absorbing Q states. Consequently, excitation energy transfer (EET) in photosynthetic pigment-protein complexes involving the B states has so far not been considered. We present, for the first time, a theoretical framework for the existence of B-B EET in tightly coupled Chl aggregates such as photosynthetic pigment-protein complexes. We show that according to a Förster resonance energy transport (FRET) scheme, unmodulated B-B EET has an unexpectedly high range. Unsuppressed, it could pose an existential threat: the damage potential of blue light for photochemical reaction centers (RCs) is well-known. This insight reveals so far undescribed roles for carotenoids (Crts, this article) and Chl b (next article in this series) of possibly vital importance. Our model system is the photosynthetic antenna pigment-protein complex (CP29). Here, we show that the B → Q IC is assisted by the optically allowed Crt state (S 2 ): The sequence is B → S 2 (Crt, unrelaxed) → S 2 (Crt, relaxed) → Q. This sequence has the advantage of preventing ∼39% of Chl-Chl B-B EET since the Crt S 2 state is a highly efficient FRET acceptor. The B-B EET range and thus the likelihood of CP29 to forward potentially harmful B excitations toward the RC are thus reduced. In contrast to the B band of Chls, most Crt energy donation is energetically located near the Q band, which allows for 74/80% backdonation (from lutein/violaxanthin) to Chls. Neoxanthin, on the other hand, likely donates in the B band region of Chl b , with 76% efficiency. Crts thus act not only in their currently proposed photoprotective roles but also as a crucial building block for any system that could otherwise deliver harmful "blue" excitations to the RCs.