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Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins

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Abstract

Plants collect light for photosynthesis using light-harvesting complexes (LHCs)—an array of chlorophyll proteins that are able to reversibly switch from harvesting to energy-dissipation mode to prevent damage of the photosynthetic apparatus. LHC antennae as well as other members of the LHC superfamily evolved from cyanobacterial ancestors called high light–inducible proteins (Hlips). Here, we characterized a purified Hlip family member HliD isolated from the cyanobacterium Synechocystis sp. PCC 6803. We found that the HliD binds chlorophyll-a (Chl-a) and β-carotene and exhibits an energy-dissipative conformation. Using femtosecond spectroscopy, we demonstrated that the energy dissipation is achieved via direct energy transfer from a Chl-a Qy state to the β-carotene S1 state. We did not detect any cation of β-carotene that would accompany Chl-a quenching. These results provide proof of principle that this quenching mechanism operates in the LHC superfamily and also shed light on the photoprotective role of Hlips and the evolution of LHC antennae.

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Figure 1: Biochemical characterization of the f.Ycf39–HliD complex.
Figure 2: Transient absorption spectroscopy of the f.Ycf39–HliD complex.
Figure 3: Transient absorption data recorded after direct excitation of β-carotene.
Figure 4: Scheme of energy transfer pathways in HliD.

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Acknowledgements

The authors thank M. Durchan and J. Tichý for their help with fluorescence measurements. J.K., T.P., V.Š. and R.S. were supported by the project P501/12/G055 from the Czech Science Foundation and by project Algatech. M.K.S. was supported by the project 14-13967S from the Czech Science Foundation and H.S. by the project CZ.1.07/2.3.00/30.0049.

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M.K.S. purified the f.Ycf39–HliD complex under the supervision of R.S.; J.K., R.K. and R.S. performed biochemical analyses. H.S. and V.Š. performed ultrafast spectroscopic experiments and analyzed data under the supervision of T.P.; R.S., T.P. and J.K. designed the study and wrote the paper. The whole study was supervised by R.S. All authors discussed the results and commented on the manuscript.

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Correspondence to Roman Sobotka.

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The authors declare no competing financial interests.

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Supplementary Results, Supplementary Table 1 and Supplementary Figures 1–8. (PDF 904 kb)

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Staleva, H., Komenda, J., Shukla, M. et al. Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol 11, 287–291 (2015). https://doi.org/10.1038/nchembio.1755

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