Rates and pathways of energy migration from the phycobilisome to the photosystem II and to the orange carotenoid protein in cyanobacteria

Krasilnikov, P. M.; Zlenko, Dmitry V.; Stadnichuk, Igor N.

doi:10.1002/1873-3468.13709

Cited by 10 publications

(10 citation statements)

References 67 publications

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“…The shortcut connecting the FRL- PBSs to the FRL-PSII RCs is likely to involve an intermediate Chl in the antenna (CP43/47 paralogs) acting as a bridge. Indeed, structural data on canonical PBSs have shown that the pigments in the APC core are too far from those of the PSII RC to allow direct energy transfer between them 8 , 9 , 33 . To allow for faster trapping of bilin excitations, this bridging Chl in the antenna needs to be better connected to the RC than most other red-shifted Chls and, to avoid energetic barriers when receiving excitations from FRL-PBSs, it is likely to be red-shifted as well.…”

Section: Discussionmentioning

confidence: 99%

The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II

et al. 2022

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Cyanobacteria carry out photosynthetic light-energy conversion using phycobiliproteins for light harvesting and the chlorophyll-rich photosystems for photochemistry. While most cyanobacteria only absorb visible photons, some of them can acclimate to harvest far-red light (FRL, 700–800 nm) by integrating chlorophyll f and d in their photosystems and producing red-shifted allophycocyanin. Chlorophyll f insertion enables the photosystems to use FRL but slows down charge separation, reducing photosynthetic efficiency. Here we demonstrate with time-resolved fluorescence spectroscopy that on average charge separation in chlorophyll-f-containing Photosystem II becomes faster in the presence of red-shifted allophycocyanin antennas. This is different from all known photosynthetic systems, where additional light-harvesting complexes increase the overall absorption cross section but slow down charge separation. This remarkable property can be explained with the available structural and spectroscopic information. The unique design is probably important for these cyanobacteria to efficiently switch between visible and far-red light.

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Section: Discussionmentioning

confidence: 99%

The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II

et al. 2022

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“…By reorganizing [1] we obtain: The k value is interpreted as an additional loss in the energy transfer efficiency with excitation using amber light compared to that with excitation using blue light and is equivalent to a change in the energy transfer efficiency from PBSs to PSII. The energy transfer efficiency is implicitly explained by Förster resonance energy transfer mechanism and determined by the distance between the PBS and PSII (Krasilnikov et al, 2020). A constant k level may therefore reflect a constant distance on average at which PBSs are detached from PSII.…”

Section: Discussionmentioning

confidence: 99%

“…If the energy transfer efficiency follows the Förster resonance energy transfer mechanism in which the efficiency is inversely proportional to the sixth power of the distance between the donor and acceptor pigment, an increase of distance by ∼10% is needed for the value of k to be 1.8. A slight shift of less than 0.5 nm in distance suffices to induce the energetic decoupling of PBSs from PSII as the shortest distance of the two pigments between the PBS and PSII is ∼4 nm (Chang et al, 2015; Krasilnikov et al, 2020). Such a mechanistic view is compatible with the previous finding that no mobile PBSs between PSII and PSI was observed in another extremophilic red alga C. caldarium using FRAP analysis (Kaňa et al, 2014), since PBS movement of less than one nanometer can result in strong energetic decoupling and is not detectable under light microscope.…”

Section: Discussionmentioning

confidence: 99%

Energetic decoupling of phycobilisomes from photosystem II involved in nonphotochemical quenching in red algae

Chiang

Huang

2022

Preprint

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To mitigate photodamage under fluctuating light conditions, photosynthetic organisms respond by regulating light energy absorbed by light-harvesting complexes and used for photochemistry. Nonphotochemical quenching acts as a frontline response to prevent excitation energy from reaching the photochemical reaction center of photosystem II. The mechanisms underlying nonphotochemical quenching in red algae, which display unique combination of light-harvesting transmembrane antenna proteins and membrane-attached phycobilisomes, appear to be different from those in cyanobacteria, green algae, and plants. Several single-process models have been proposed for red algal nonphotochemical quenching, yet the possibility of more than one process being involved in nonphotochemical quenching awaits further investigation. To assess multiple nonphotochemical quenching processes in the extremophilic red alga Cyanidioschyzon merolae, fluorescence analyses with light preferentially absorbed by phycobilisomes or photosystems were utilized. Energetic decoupling of phycobilisomes from photosystem II and intrinsic photosystem II quenching were identified as two dominant processes involved in nonphotochemical quenching and distinguished by their kinetics. Whereas the degrees of energetic decoupling remained similar after its induction, the degrees of intrinsic photosystem II quenching varied depending on the illumination period and intensity. The respective effects of protein crosslinkers, osmolytes, ionophores, and photosynthetic inhibitors on the kinetics of nonphotochemical quenching suggested that the energetic decoupling involved conformational changes associated with the connection between the PBS and PSII. Furthermore, the surface charge on the thylakoid membrane played a significant role in the modulation of red algal nonphotochemical quenching.

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“…The implemented in (Krasilnikov et al 2020) model of PBS docking to the PS II dimer on the surface of the thylakoid membrane was tested for the possibility of energy transfer via the PBLcm energy channel and for agreement between the calculated and experimental transfer times. The excitonic coupling model of the OCP and PBLcm interaction, previously well established (Krasilnikov et al 2020;Stadnichuk et al 2015), was then revised in accordance with the course of energy transfer from PBLcm to PS II, as well as the PBS to OCP cell ratio. In this way, we show that, within the framework of the model constructed, the times of energy transfer from the PBLcm to the PS II and from the PBLcm to the OCP are closely correlated.…”

Section: Introductionmentioning

confidence: 99%

“…2015;Krasilnikov et al 2020). Considering the thickness of the apoprotein layer over the near-surface chlorophylls of PS II and the gap created by this protrusion and the amorphous PBLcm loop exposed from the PBS core towards the thylakoid membrane, the distance of 42 Å most likely offered by the model(Krasilnikov et al 2020) was used here to provide an opportunity for energy transfer from PBS to PS II.…”

mentioning

confidence: 99%

Relationship between non-photochemical quenching efficiency and the energy transfer rate from phycobilisomes to photosystem II

Stadnichuk

Krasilnikov

2023

Photosynth Res

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The chromophorylated PBLcm domain of the ApcE linker protein in the cyanobacterial phycobilisome (PBS) serves as a bottleneck for Förster resonance energy transfer (FRET) from the PBS to the antennal chlorophyll of photosystem II (PS II) and as a redirection point for energy distribution to the orange protein ketocarotenoid (OCP), which is excitonically coupled to the PBLcm chromophore in the process of non-photochemical quenching (NPQ) under high light conditions. The involvement of PBLcm in the quenching process was rst directly demonstrated by measuring steady-state uorescence spectra of cyanobacterial cells at different stages of NPQ development. The time required to transfer energy from the PBLcm to the OCP is several times shorter than the time it takes to transfer energy from the PBLcm to the PS II, ensuring quenching e ciency. The data obtained provide an explanation for the different rates of PBS quenching in vivo and in vitro according to the half ratio of OCP/PBS in the cyanobacterial cell, which is tens of times lower than that realised for an effective NPQ process in solution.

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Rates and pathways of energy migration from the phycobilisome to the photosystem II and to the orange carotenoid protein in cyanobacteria

Cited by 10 publications

References 67 publications

The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II

The antenna of far-red absorbing cyanobacteria increases both absorption and quantum efficiency of Photosystem II

Energetic decoupling of phycobilisomes from photosystem II involved in nonphotochemical quenching in red algae

Relationship between non-photochemical quenching efficiency and the energy transfer rate from phycobilisomes to photosystem II

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