Excitation energy transfer between higher excited states of photosynthetic pigments: 1. Carotenoids facilitate B -> Q band conversion in chlorophylls

Chlorophylls (Chls) are known for fast, sub-picosecond 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 simple Forster resonance energy transport (FRET) scheme, unmodulated B-B EET likely poses an existential threat, in particular the photochemical reaction centers (RCs). This insight leads to so-far undescribed roles for carotenoids (Crts, this article) and Chl b (next article in this series) of possibly primary importance. Here we show that B [->] Q IC is assisted by the symmetry-allowed Crt state (S2) by using the plant antenna complex CP29 as a model: The sequence is B [->] S2 (Crt, unrelaxed) [->]S2 (Crt, relaxed) [->] Q. This sequence has the advantage of preventing ~ 39% of Chl-Chl B-B EET, since the Crt S2 state is a highly efficient FRET acceptor. The likelihood of CP29 to forward potentially harmful B excitations towards the photosynthetic reaction center (RC) is 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. The latter is discussed in more detail in the next article in this series. Crts thus do not only act 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.