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Phycobilisome integrity and functionality in lipid unsaturation and xanthophyll mutants in Synechocystis

Abstract

The major light-harvesting system in cyanobacteria, the phycobilisome, is an essential component of the photosynthetic apparatus that regulates the utilization of the natural light source—the Sun. Earlier works revealed that the thylakoid membrane composition and its physical properties might have an important role in antennas docking. Polyunsaturated lipids and xanthophylls are among the most significant modulators of the physical properties of thylakoid membranes. In the nature, the action of these molecules is orchestrated in response to environmental stimuli among which the growth temperature is the most influential. In order to further clarify the significance of thylakoid membrane physical properties for the phycobilisomes assembly (i.e. structural integrity) and their ability to efficiently direct the excitation energy towards the photosynthetic complexes, in this work, we utilize cyanobacterial Synechocystis sp. PCC 6803 mutants deficient in polyunsaturated lipids (AD mutant) and xanthophylls (RO mutant), as well as a strain depleted of both xanthophylls and polyunsaturated lipids (ROAD multiple mutant). For the first time, we discuss the effect of those mutations on the phycobilisomes assembly, integrity and functionality at optimal (30 °C) and moderate low (25 °C) and high (35 °C) temperatures. Our results show that xanthophyll depletion exerts a much stronger effect on both phycobilisome’s integrity and the response of cells to growth at suboptimal temperatures than lipid unsaturation level. The strongest effects were observed for the combined ROAD mutant, which exhibited thermally destabilized phycobilisomes and a population of energetically uncoupled phycocyanin units.

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Acknowledgements

The authors would like to acknowledge Prof. Zoltan Gombos who initiated this project, but has sadly deceased during the completion of this work. The authors of the manuscript are in-depth of his scientific wisdom, uniqueness and enthusiasm to discover the essential role of various lipids and membrane components for cyanobacterial photosynthetic processes. The authors are grateful to Dr. Mihály Kis for the generation of ROAD mutant. This work was also supported by a fruitful bilateral collaboration program between the Bulgarian and Hungarian Academy of Sciences for the period 2015–2018. N.P. is thankful to the National Research Programme “Young scientists and postdoctoral students” approved by DCM # 577/17.08.2018 for the support granted.

Funding

This work is supported by National Research Programme “Young scientists and postdoctoral students” approved by DCM # 577/17.08.2018, Ministry of Education and Science of Bulgaria (N.P.), bilateral exchange visit program between the Bulgarian and Hungarian Academy of Sciences (S.K, Z.G.), and the Hungarian Scientific Research Fund, Hungarian Government Grant GINOP-2.3.2-15-2016-00001 (Z.G.).

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ZG, HL-D, TT and SK contributed conception and design of the study; EH, HL-D TK and TZ cultivated cells and performed absorption spectroscopy; SV and TT performed and analyzed 77 K fluorescence measurements; SJT and NP measured and analyzed the differential scanning calorimetry profiles; SGT, KL supervised the experimental work and corrected parts of the manuscript; SK, KL and TT wrote the paper. All authors contributed to manuscript revision.

Corresponding author

Correspondence to Sashka Krumova.

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This work is supported by the following research grants: National Research Programme “Young scientists and postdoctoral students” approved by DCM # 577/17.08.2018, Ministry of Education and Science of Bulgaria (N.P.), bilateral exchange visit program between the Bulgarian and Hungarian Academy of Sciences (S.K, Z.G.), and the Hungarian Scientific Research Fund, Hungarian Government Grant GINOP-2.3.2-15-2016-00001 (Z.G.).

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Vajravel, S., Laczkó-Dobos, H., Petrova, N. et al. Phycobilisome integrity and functionality in lipid unsaturation and xanthophyll mutants in Synechocystis. Photosynth Res 145, 179–188 (2020). https://doi.org/10.1007/s11120-020-00776-1

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Keywords

  • Phycobilisome
  • Cyanobacteria
  • Lipid unsaturation
  • Carotenoids
  • Excitation energy transfer
  • Thermal stability