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

Abstract

AbstractChlorophylls (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 Förster 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 Chlb(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 S2state 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 Chlb, 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.