Photosynthetica 2023, 61(3):308-317 | DOI: 10.32615/ps.2023.022
Evaluation of the relationship between color-tuning of photosynthetic excitons and thermodynamic stability of light-harvesting chromoproteins
- 1 Institute of Physics, University of Tartu, W. Ostwaldi 1, 50411 Tartu, Estonia
- 2 Faculty of Science, Ibaraki University, 310-8512 Mito, Japan
- 3 Estonian Academy of Sciences, Kohtu 6, 10130 Tallinn, Estonia
Color-tuning is a critical survival mechanism for photosynthetic organisms. Calcium ions are believed to enhance both spectral tuning and thermostability in obligatory calcium-containing sulfur purple bacteria. This study examined the thermo- and piezo stability of the LH1-RC complexes from two calcium-containing sulfur purple bacteria notable for their extreme red-shifted spectra. The results generally show limited reversibility of both temperature and pressure effects related to the malleability of calcium-binding sites. While the pressure-induced decomposition product closely resembles the calcium-depleted form of the chromoproteins, the thermally induced products reveal monomeric B777 and dimeric B820 forms of bacteriochlorophyll a, similar to those seen in non-sulfur purple bacteria treated with detergent. The study further found nearly unison melting of the protein tertiary and secondary structures. Overall, our findings do not support a direct link between color adjustment and thermodynamic stability in light-harvesting chromoproteins.
Additional key words: Ca-containing bacteria; circular dichroism; hydrostatic high pressure; LH1-RC complex; purple bacteria.
Received: April 17, 2023; Revised: April 17, 2023; Accepted: May 17, 2023; Prepublished online: June 1, 2023; Published: October 5, 2023 Show citation
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References
- Chang M.C., Callahan P.M., Parkes-Loach P.S. et al.: Spectroscopic characterization of the light-harvesting complex of Rhodospirillum rubrum and its structural subunit. - Biochemistry 29: 421-429, 1990.
Go to original source... - Cogdell R.J., Isaacs N.W., Freer A.A. et al.: The structure and function of the LH2 (B800-850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050. - Prog. Biophys. Mol. Biol. 68: 1-27, 1997.
Go to original source... - Di Bari D., Timr S., Guiral M. et al.: Diffusive dynamics of bacterial proteome as a proxy of cell death. - ACS Centr. Sci. 9: 93-102, 2023.
Go to original source... - Fiedor L., Scheer H.: Trapping of an assembly intermediate of photosynthetic LH1 antenna beyond B820 subunit: Significance for the assambly of photosynthetic LH1 antenna. -J. Biol. Chem. 280: 20921-20926, 2005.
Go to original source... - Freiberg A., Ellervee A., Kukk P. et al.: Pressure effects on spectra of photosynthetic light-harvesting pigment-protein complexes. - Chem. Phys. Lett. 214: 10-16, 1993.
Go to original source... - Freiberg A., Kangur L., Olsen J.D., Hunter C.N.: Structural implications of hydrogen-bond energetics in membrane proteins revealed by high-pressure spectroscopy. - Biophys. J. 103: 2352-2360, 2012.
Go to original source... - Georgakopoulou S., van der Zwan G., Olsen J.D. et al.: Investigation of the effects of different carotenoids on the absorption and CD signals of light harvesting 1 complexes. - J. Phys. Chem. B 110: 3354-3361, 2006.
Go to original source... - Imanishi M., Takenouchi M., Takaichi S. et al.: A dual role for Ca2+ in expanding the spectral diversity and stability of light-harvesting 1 reaction center photocomplexes of purple phototrophic bacteria. - Biochemistry 58: 2844-2852, 2019.
Go to original source... - Kangur L., Rätsep M., Timpmann K. et al.: The two light-harvesting membrane chromoproteins of Thermochromatium tepidum expose distinct robustness against temperature and pressure. - BBA-Bioenergetics 1861: 148205, 2020.
Go to original source... - Kangur L., Timpmann K., Freiberg A.: Stability of integral membrane proteins against high hydrostatic pressure: the LH2 and LH3 antenna pigment-protein complexes from photosynthetic bacteria. - J. Phys. Chem. B 112: 7948-7955, 2008.
Go to original source... - Kimura Y., Hirano Y., Yu L.-J. et al.: Calcium ions are involved in the unusual red shift of the light-harvesting 1 Qy transition of the core complex in thermophilic purple sulfur bacterium Thermochromatium tepidum. - J. Biol. Chem. 283: 13867-13873, 2008.
Go to original source... - Kimura Y., Tani K., Madigan M.T., Wang-Otomo Z.-Y.: Advances in the spectroscopic and structural characterization of core light-harvesting complexes from purple phototrophic bacteria. - J. Phys. Chem. B 127: 6-17, 2023.
Go to original source... - Kimura Y., Yu L.-J., Hirano Y. et al.: Calcium ions are required for the enhanced thermal stability of the light-harvesting-reaction center core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum. - J. Biol. Chem. 284: 93-99, 2009.
Go to original source... - Leiger K., Linnanto J.M., Rätsep M. et al.: Controlling photosynthetic excitons by selective pigment photooxidation. - J. Phys. Chem. B 123: 29-38, 2019.
Go to original source... - Luke K.A., Higgins C.L., Wittung-Stafshede P.: Thermodynamic stability and folding of proteins from hyperthermophilic organisms. - FEBS J. 274: 4023-4033, 2007.
Go to original source... - Matsuo K., Sakurada Y., Yonehara R. et al.: Secondary-structure analysis of denatured proteins by vacuum-ultraviolet circular dichroism spectroscopy. - Biophys. J. 92: 4088-4096, 2007.
Go to original source... - Michalik M., Zbyradowski M., Heriyanto, Fiedor L.: Tuning the photophysical features of self-assembling photoactive polypeptides for light-harvesting. - Materials 12: 3554, 2019.
Go to original source... - Nozawa T., Trost J.T., Fukada T. et al.: Properties of the reaction center of the thermophilic purple photosynthetic bacterium Chromatium tepidum. - BBA-Bioenergetics 894: 468-476, 1987.
Go to original source... - Pandit A., van Stokkum I.H.M., Georgakopoulou S. et al.: Investigations of intermediates appearing in the reassociation of the light-harvesting 1 complex of Rhodospirillum rubrum. -Photosynth. Res. 75: 235-248, 2003.
Go to original source... - Parkes-Loach P.S., Sprinkle J.R., Loach P.A.: Reconstitution of the B873 light-harvesting complex of Rhodospirillum rubrum from the separately isolated α- and β-polypeptides and bacteriochlorophyll a. - Biochemistry 27: 2718-2727, 1988.
Go to original source... - Permentier H.P., Neerken S., Overmann J., Amesz J.: A bacteriochlorophyll a antenna complex from purple bacteria absorbing at 963 nm. - Biochemistry 40: 5573-5578, 2001.
Go to original source... - Polyakov I.V., Khrenova M.G., Moskovsky A.A. et al.: Towards first-principles calculation of electronic excitations in the ring of the protein-bound bacteriochlorophylls. - Chem. Phys. 505: 34-39, 2018.
Go to original source... - Puusepp M., Kangur L., Freiberg A.: Dissociation of the light-harvesting membrane protein complex I from Rhodobacter sphaeroides under high hydrostatic pressure. - High Press. Res. 35: 176-180, 2015.
Go to original source... - Rätsep M., Muru R., Freiberg A.: High temperature limit of photosynthetic excitons. - Nat. Commun. 9: 99, 2018.
Go to original source... - Reppert M.: Bioexcitons by design: How do we get there? - J. Phys. Chem. B 127: 1872-1879, 2023.
Go to original source... - Sancho J.: The stability of 2-state, 3-state and more-state proteins from simple spectroscopic techniques... Plus the structure of the equilibrium intermediates at the same time. - Arch. Biochem. Biophys. 531: 4-13, 2013.
Go to original source... - Smith J.R.L., Calvin M.: Studies of the chemical and photochemical oxidation of bacteriochlorophyll. - J. Am. Chem. Soc. 88: 4500-4506, 1966.
Go to original source... - ©tìpánek P., Bouø P.: Multi-scale modeling of electronic spectra of three aromatic amino acids: Importance of conformational averaging and explicit solute-solvent interactions. - Phys. Chem. Chem. Phys. 16: 20639-20649, 2014.
Go to original source... - Suzuki H., Hirano Y., Kimura Y. et al.: Purification, characterization and crystallization of the core complex from thermophilic purple sulfur bacterium Thermochromatium tepidum. - BBA-Bioenergetics 1767: 1057-1063, 2007.
Go to original source... - Tani K., Kanno R., Makino Y. et al.: Cryo-EM structure of a Ca2+-bound photosynthetic LH1-RC complex containing multiple αβ-polypeptides. - Nat. Commun. 11: 4955, 2020.
Go to original source... - Timpmann K., Kangur L., Freiberg A.: Hysteretic pressure dependence of Ca2+ binding in LH1 bacterial membrane chromoproteins. - J. Phys. Chem. B 127: 456-464, 2023.
Go to original source... - Timpmann K., Rätsep M., Kangur L. et al.: Exciton origin of color-tuning in Ca2+-binding photosynthetic bacteria. - Int. J. Mol. Sci. 22: 7338, 2021.
Go to original source... - Visschers R.W., Nunn R., Calkoen F. et al.: Spectroscopic characterization of B820 subunits from light-harvesting complex I of Rhodospirillum rubrum and Rhodobacter sphaeroides prepared with the detergent n-octyl-rac-2,3-dipropylsulfoxide. - BBA-Bioenergetics 1100: 259-266, 1992.
Go to original source... - Visschers R.W., van Grondelle R., Robert B.: Resonance Raman spectroscopy of the B820 subunit of the core antenna from Rhodospirillum rubrum G9. - BBA-Bioenergetics 1183: 369-373, 1993.
Go to original source... - Yu L.-J., Kawakami T., Kimura Y., Wang-Otomo Z.-Y.: Structural basis for the unusual Qy red-shift and enhanced thermostability of the LH1 complex from Thermochromatium tepidum. - Biochemistry 55: 6495-6504, 2016.
Go to original source... - Yu L.-J., Suga M., Wang-Otomo Z.-Y., Shen J.-R.: Structure of photosynthetic LH1-RC supercomplex at 1.9 Å resolution. - Nature 556: 209-213, 2018.
Go to original source...




