Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

Abstract

<pre><p><a></a>Green plants prevent photodamage under high light conditions by dissipating excess energy as heat. Conformational changes of the photosynthetic antenna complexes activate dissipation by leveraging the sensitivity of the photophysics of the chlorophyll and carotenoids to their surrounding protein. However, the mechanisms and site of dissipation are still debated, largely due to two challenges. First, because of the ultrafast timescales and large energy gaps involved, measurements lacked the temporal or spectral requirements. Second, experiments have been performed in detergent, which can induce non-native conformations, or <i>in vivo</i>, where contributions from the multiple complexes cannot be disentangled and are further obfuscated by laser-induced artifacts. Here, we overcome both challenges by applying ultrabroadband two-dimensional electronic spectroscopy to the principal antenna complex, light-harvesting complex II, in a near-native membrane. The membrane enhances two dissipative pathways, one of which was previously uncharacterized chlorophyll-to-carotenoid energy transfer. Our results highlight the sensitivity of the photophysics to the local environment, which may be used to control the balance between light harvesting and dissipation <i>in vivo</i>.</p></pre>

Charge transfer from the carotenoid can quench chlorophyll excitation in antenna complexes of plants

“…Indeed, experimental and computational results suggest that LHCII explores several conformations in solution 17,32 . However, little is known about the behavior of the antenna in the photosynthetic membrane, which has been compared with the detergent environment only in recent experiments 26 . In order to understand the in vivo quenching mechanism of LHCII, the unquenched conformations of LHCII in the membrane need to be thoroughly characterized by a joint computational and experimental effort.…”

“…In this contribution, we fill this gap, and show that electron transfer from carotenoids can be a rapid quenching pathway for excited Chl, and that it can compete with the EET to the S 1 state. To prove this hypothesis, we have focused on the major light-harvesting complex II (LCHII) of plants, for which previous studies have already shown the effectiveness of the EET mechanism 7,9,10,26 .…”

Mechanisms shaping the synergism of zeaxanthin and PsbS in photoprotective energy dissipation in the photosynthetic apparatus of plants

“…This suggests the operation of a mechanism in which modulation of excitation quenching is rather realized in the thylakoid membranes indirectly, e.g. via the influence on a molecular organization of the pigment-protein complexes or by modifying their immediate environment (Ruban et al, 1997;Gruszecki et al, 2006;Johnson et al, 2011;Xu et al, 2015;Welc et al, 2016;Son et al, 2020b;Zhou et al, 2020). The results of the experiments have been presented, showing that both Zea (Ruban et al, 1997;Gruszecki et al, 2006;Zhou et al, 2020) and PsbS (Sacharz et al, 2017) influence molecular organization of LHCII.…”

“…This shows that, Figure 7). In our opinion, it is highly probable that such a control of excitation quenching in LHCII is mechanistically realized via influencing the conformation and dynamics in the complex, directly associated with the photophysical processes, including excitation energy transfer to the S1 state of carotenoids (Son et al, 2020b;Son et al, 2020a). plants results in the increase of availability of Vio for enzymatic deepoxidation ( Figure 1A).…”

“…Recently, it has been demonstrated that both those mechanisms, the chlorophyll-carotenoid excitation energy transfer and the charge transfer can operate simultaneously as elements of regulatory activity in alga Nannochloropsis oceanica (Park et al, 2019). The singlet-singlet excitation energy transfer between the Q y level of Chl a and the S1 level of carotenoids has been recently reported to operate in an intact trimeric structure of LHCII in the lipid environment (Son et al, 2020b). On the other hand, it has been shown that the replacement of Vio to Zea in the Vio-binding site of LHCII does not essentially influence the photophysical processes in the complex (Son et al, 2020a).…”