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

Abstract

Chlorophylls (Chls) are known for fast, subpicosecond internal conversion (IC) from ultraviolet/blue-absorbing ("B" or "Soret" states) to the energetically lower, red lightabsorbing 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 Forster 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.

Excitation Energy Transfer between Higher Excited States of Photosynthetic Pigments: 2. Chlorophyll b is a B Band Excitation Trap

“…B band EET larger than 10% to other Chls a is only found for Chls 602, 609, 611, 615, and 616. Including additional PSII supercomplex pigment–proteins will likely reduce the B–B EET even for those pigments, as was shown in the previous article in this series . Associated complementary calculations are running in our lab.…”

“…B Band EET Network in CP29. In the previous article in the series, 39 a general assessment of EET in the B band region of CP29 was presented. Here, efficiencies for EET to different pigment classes are shown in more detail (Figure 3; for source values, see previous article in this series 39 ).…”

“…In the previous article in the series, 39 a general assessment of EET in the B band region of CP29 was presented. Here, efficiencies for EET to different pigment classes are shown in more detail (Figure 3; for source values, see previous article in this series 39 ). It can be seen The high preference for Chl b acceptors is likely due to the remarkable spectral identity of the Chl b B band absorption with Chl a B band emission mentioned above, as observed in the work by Leupold et al, 43 leading to the strong J B−B and larger R 0,B−B for the B band (see previous sections).…”

“…The underlying coupling can be modeled on the basis of dipole–dipole interactions by Förster resonance energy transfer (FRET) using a point dipole approximation (PDA). − For the B band, there have been very few efforts so far to elucidate EET processes (Supporting Information). However, even assuming ultrafast IC, coherent and incoherent EET have been shown to occur among B states of Zn-porphyrins (analogues of Chls), see Supporting Information. − More details on the employed approach, especially its potential shortcomings for carotenoids (Crts), can be found in the previous article in this series . We have, however, recently presented evidence that higher level incoherent EET models perform equivalently to FRET when considering ensembles such as the antenna studied here …”

“…Recently, it was also (computationally) proposed for CP29 that the coupling pattern between Chls is state-dependent and steered by the protein environment. 45 In the previous article in this series, 39 these insights were put to the test, and it was shown that B−B EET appears to be a significant process in a CP29 FRET model. The main result was that B−B EET is strongly affected by the presence of Crts.…”