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Color-Tuning Mechanism of the Lit Form of Orange Carotenoid Protein

  • Man-Hyuk Han (Department of Physics, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Hee Wook Yang (Department of Biological Sciences, Chungnam National University) ;
  • Jungmin Yoon (Department of Biological Sciences, KI for the BioCentury, KAIST) ;
  • Yvette Villafani (Department of Biological Sciences, Chungnam National University) ;
  • Ji-Young Song (Department of Biological Sciences, Chungnam National University) ;
  • Cheol Ho Pan (Natural Product Informatics Research Center, KIST Gangneung Institute of Natural Products) ;
  • Keunwan Park (Natural Product Informatics Research Center, KIST Gangneung Institute of Natural Products) ;
  • Youngmoon Cho (Department of Physics, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Ji-Joon Song (Department of Biological Sciences, KI for the BioCentury, KAIST) ;
  • Seung Joong Kim (Department of Physics, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Youn-Il Park (Department of Biological Sciences, Chungnam National University) ;
  • Jiyong Park (Center for Catalytic Hydrocarbon Functionalizations, Institute for Basic Science (IBS))
  • 투고 : 2022.11.30
  • 심사 : 2023.07.13
  • 발행 : 2023.08.31

초록

Orange carotenoid protein (OCP) of photosynthetic cyanobacteria binds to ketocarotenoids noncovalently and absorbs excess light to protect the host organism from light-induced oxidative damage. Herein, we found that mutating valine 40 in the α3 helix of Gloeocapsa sp. PCC 7513 (GlOCP1) resulted in blue- or red-shifts of 6-20 nm in the absorption maxima of the lit forms. We analyzed the origins of absorption maxima shifts by integrating X-ray crystallography, homology modeling, molecular dynamics simulations, and hybrid quantum mechanics/molecular mechanics calculations. Our analysis suggested that the single residue mutations alter the polar environment surrounding the bound canthaxanthin, thereby modulating the degree of charge transfer in the photoexcited state of the chromophore. Our integrated investigations reveal the mechanism of color adaptation specific to OCPs and suggest a design principle for color-specific photoswitches.

키워드

과제정보

This work was supported by grants from the KIST Open Research Program (2E30642-20-152) and the KRIBB Research Initiative Program (KGM1002311) in Korea to Y.I.P.; the Institute for Basic Science (IBS-R010-A1) in Korea to J.P.; the KAIST Grand Challenge 30 project (KC30) to J.J.S.; the National Research Foundation of Korea (NRF-2020R1A2B5B03001517) to J.J.S.; KC30 (N11200138) to M.H.H.; and the Korea Advanced Institute of Science and Technology (KAIST; G04180038), the National Research Foundation of Korea (NRF; 2020R1A2C1013246, 2020K1A3A7A09080399, and 2020R1A4A3079755), and the Basic Science Research Program through NRF (2019R1A6A1A10073887) to S.J.K.

참고문헌

  1. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. (2010). PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66(Pt 2), 213-221. https://doi.org/10.1107/S0907444909052925
  2. Andreoni, A., Lin, S., Liu, H., Blankenship, R.E., Yan, H., and Woodbury, N.W. (2017). Orange carotenoid protein as a control element in an antenna system based on a DNA nanostructure. Nano Lett. 17, 1174-1180. https://doi.org/10.1021/acs.nanolett.6b04846
  3. Bao, H., Melnicki, M.R., and Kerfeld, C.A. (2017a). Structure and functions of orange carotenoid protein homologs in cyanobacteria. Curr. Opin. Plant Biol. 37, 1-9. https://doi.org/10.1016/j.pbi.2017.03.010
  4. Bao, H., Melnicki, M.R., Pawlowski, E.G., Sutter, M., Agostoni, M., Lechno-Yossef, S., Cai, F., Montgomery, B.L., and Kerfeld, C.A. (2017b). Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria. Nat. Plants 3, 17089.
  5. Bayly, C.I., Cieplak, P., Cornell, W.D., and Kollman, P.A. (1993). A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: the RESP model. J. Phys. Chem. 97, 10269-10280. https://doi.org/10.1021/j100142a004
  6. Becke, A.D. (1993). A new mixing of hartree-fock and local density-functional theories. J. Chem. Phys. 98, 1372-1377. https://doi.org/10.1063/1.464304
  7. Binkley, J.S., Pople, J.A., and Hehre, W.J. (1980). Self-consistent molecular-orbital methods. 21. Small split-valence basis-sets for 1st-row elements. J. Am. Chem. Soc. 102, 939-947. https://doi.org/10.1021/ja00523a008
  8. Bondanza, M., Cupellini, L., Lipparini, F., and Mennucci, B. (2020). The multiple roles of the protein in the photoactivation of orange carotenoid protein. Chem 6, 187-203. https://doi.org/10.1016/j.chempr.2019.10.014
  9. Caffrey, D.R., Dana, P.H., Mathur, V., Ocano, M., Hong, E.J., Wang, Y.E., Somaroo, S., Caffrey, B.E., Potluri, S., and Huang, E.S. (2007). PFAAT version 2.0: a tool for editing, annotating, and analyzing multiple sequence alignments. BMC Bioinformatics 8, 381.
  10. Case, D.A., Cheatham, T.E., 3rd, Darden, T., Gohlke, H., Luo, R., Merz, K.M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R.J. (2005). The amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688. https://doi.org/10.1002/jcc.20290
  11. Christensen, R.L. (1999). The electronic states of carotenoids. In The Photochemistry of Carotenoids, H.A. Frank, A.J. Young, G. Britton, and R.J. Cogdell, eds. (Dordrecht, Netherlands: Springer), pp. 137-159.
  12. de Carbon, C.B., Thurotte, A., Wilson, A., Perreau, F., and Kirilovsky, D. (2015). Biosynthesis of soluble carotenoid holoproteins in Escherichia coli. Sci. Rep. 5, 9085.
  13. Dominguez-Martin, M.A. and Kerfeld, C.A. (2019). Engineering the orange carotenoid protein for applications in synthetic biology. Curr. Opin. Struct. Biol. 57, 110-117. https://doi.org/10.1016/j.sbi.2019.01.023
  14. Efron, B. and Tibshirani, R. (1986). Bootstrap methods for standard errors, confidence intervals, and other measures of statistical accuracy. Stat. Sci. 1, 54-77. https://doi.org/10.1214/ss/1177013815
  15. Emsley, P. and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60(Pt 12 Pt 1), 2126-2132. https://doi.org/10.1107/S0907444904019158
  16. Fiedor, L., Heriyanto, Fiedor, J., and Pilch, M. (2016). Effects of molecular symmetry on the electronic transitions in carotenoids. J. Phys. Chem. Lett. 7, 1821-1829. https://doi.org/10.1021/acs.jpclett.6b00637
  17. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G.A., et al. (2009). Gaussian 09, Revision D.01 (Wallingford: Gaussian Inc.).
  18. Grant, B.J., Rodrigues, A.P.C., ElSawy, K.M., McCammon, J.A., and Caves, L.S.D. (2006). Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22, 2695-2696. https://doi.org/10.1093/bioinformatics/btl461
  19. Griffiths, D.J. and Schroeter, D.F. (2018). Introduction to Quantum Mechanics (3rd Edition) (Cambridge: Cambridge University Press).
  20. Grimme, S., Antony, J., Ehrlich, S., and Krieg, H. (2010). A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu. J. Chem. Phys. 132, 154104.
  21. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307-321. https://doi.org/10.1093/sysbio/syq010
  22. Gwizdala, M., Wilson, A., and Kirilovsky, D. (2011). In vitro reconstitution of the cyanobacterial photoprotective mechanism mediated by the orange carotenoid protein in Synechocystis PCC 6803. Plant Cell 23, 2631-2643. https://doi.org/10.1105/tpc.111.086884
  23. Humphrey, W., Dalke, A., and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38. https://doi.org/10.1016/0263-7855(96)00018-5
  24. Hyun, Y., Baek, Y., Lee, C., Ki, N., Ahn, J., Ryu, S., and Ha, N.C. (2021). Structure and function of the autolysin SagA in the type IV secretion system of Brucella abortus. Mol. Cells 44, 517-528. https://doi.org/10.14348/molcells.2021.0011
  25. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., and Klein, M.L. (1983). Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935. https://doi.org/10.1063/1.445869
  26. Kerfeld, C.A., Melnicki, M.R., Sutter, M., and Dominguez-Martin, M.A. (2017). Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. New Phytol. 215, 937-951. https://doi.org/10.1111/nph.14670
  27. Kerfeld, C.A., Sawaya, M.R., Brahmandam, V., Cascio, D., Ho, K.K., Trevithick-Sutton, C.C., Krogmann, D.W., and Yeates, T.O. (2003). The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11, 55-65. https://doi.org/10.1016/S0969-2126(02)00936-X
  28. Kim, T., Kim, W., Vakuliuk, O., Gryko, D.T., and Kim, D. (2020). Two-step charge separation passing through the partial charge-transfer state in a molecular dyad. J. Am. Chem. Soc. 142, 1564-1573. https://doi.org/10.1021/jacs.9b12016
  29. Kirilovsky, D. and Kerfeld, C.A. (2013). The orange carotenoid protein: a blue-green light photoactive protein. Photochem. Photobiol. Sci. 12, 1135-1143. https://doi.org/10.1039/c3pp25406b
  30. Kirilovsky, D. and Kerfeld, C.A. (2016). Cyanobacterial photoprotection by the orange carotenoid protein. Nat. Plants 2, 16180.
  31. Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549. https://doi.org/10.1093/molbev/msy096
  32. Kuznetsova, V., Dominguez-Martin, M.A., Bao, H., Gupta, S., Sutter, M., Kloz, M., Rebarz, M., Precek, M., Chen, Y., Polivka, T., et al. (2020). Comparative ultrafast spectroscopy and structural analysis of OCP1 and OCP2 from Tolypothrix. Biochim. Biophys. Acta Bioenerg. 1861, 148120.
  33. Letunic, I. and Bork, P. (2019). Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47(W1), W256-W259. https://doi.org/10.1093/nar/gkz239
  34. Leverenz, R.L., Sutter, M., Wilson, A., Gupta, S., Thurotte, A., De Carbon, C.B., Petzold, C.J., Ralston, C., Perreau, F., Kirilovsky, D., et al. (2015). A 12 A carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348, 1463-1466. https://doi.org/10.1126/science.aaa7234
  35. Liang, M.H., Zhu, J., and Jiang, J.G. (2018). Carotenoids biosynthesis and cleavage related genes from bacteria to plants. Crit. Rev. Food Sci. Nutr. 58, 2314-2333. https://doi.org/10.1080/10408398.2017.1322552
  36. Liu, H., Zhang, H., Orf, G.S., Lu, Y., Jiang, J., King, J.D., Wolf, N.R., Gross, M.L., and Blankenship, R.E. (2016). Dramatic domain rearrangements of the cyanobacterial orange carotenoid protein upon photoactivation. Biochemistry 55, 1003-1009. https://doi.org/10.1021/acs.biochem.6b00013
  37. Maier, J.A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K.E., and Simmerling, C. (2015). ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB. J. Chem. Theory Comput. 11, 3696-3713. https://doi.org/10.1021/acs.jctc.5b00255
  38. Martin, R.L. (2003). Natural transition orbitals. J. Chem. Phys. 118, 4775- 4777. https://doi.org/10.1063/1.1558471
  39. Melnicki, M.R., Leverenz, R.L., Sutter, M., Lopez-Igual, R., Wilson, A., Pawlowski, E.G., Perreau, F., Kirilovsky, D., and Kerfeld, C.A. (2016). Structure, diversity, and evolution of a new family of soluble carotenoid-binding proteins in cyanobacteria. Mol. Plant 9, 1379-1394. https://doi.org/10.1016/j.molp.2016.06.009
  40. Moldenhauer, M., Sluchanko, N.N., Buhrke, D., Zlenko, D.V., Tavraz, N.N., Schmitt, F.J., Hildebrandt, P., Maksimov, E.G., and Friedrich, T. (2017). Assembly of photoactive orange carotenoid protein from its domains unravels a carotenoid shuttle mechanism. Photosynth. Res. 133, 327-341. https://doi.org/10.1007/s11120-017-0353-3
  41. Muzzopappa, F. and Kirilovsky, D. (2020). Changing color for photoprotection: the orange carotenoid protein. Trends Plant Sci. 25, 92-104. https://doi.org/10.1016/j.tplants.2019.09.013
  42. Muzzopappa, F., Wilson, A., and Kirilovsky, D. (2019). Interdomain interactions reveal the molecular evolution of the orange carotenoid protein. Nat. Plants 5, 1076-1086. https://doi.org/10.1038/s41477-019-0514-9
  43. Otwinowski, Z. and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. https://doi.org/10.1016/S0076-6879(97)76066-X
  44. Park, S.S., Lee, S., and Rhee, D.K. (2021). Crystal structure of the pneumococcal vancomycin-resistance response regulator DNA-binding domain. Mol. Cells 44, 179-185. https://doi.org/10.14348/molcells.2021.2235
  45. R Core Team (2015). R: A Language and Environment for Statistical Computing (Vienna: R Foundation for Statistical Computing).
  46. Rocha-Rinza, T., Christiansen, O., Rajput, J., Gopalan, A., Rahbek, D.B., Andersen, L.H., Bochenkova, A.V., Granovsky, A.A., Bravaya, K.B., Nemukhin, A.V., et al. (2009). Gas phase absorption studies of photoactive yellow protein chromophore derivatives. J. Phys. Chem. A 113, 9442-9449. https://doi.org/10.1021/jp904660w
  47. Sanchez, R., Serra, F., Tarraga, J., Medina, I., Carbonell, J., Pulido, L., de Maria, A., Capella-Gutierrez, S., Huerta-Cepas, J., Gabaldon, T., et al. (2011). Phylemon 2.0: a suite of web-tools for molecular evolution, phylogenetics, phylogenomics and hypotheses testing. Nucleic Acids Res. 39(Web Server issue), W470-W474. https://doi.org/10.1093/nar/gkr408
  48. Schrodinger, L. (2016). The PyMOL Molecular Graphics System, Version 2.4.1 (New York: Schrodinger, LLC).
  49. Senn, H.M. and Thiel, W. (2007). QM/MM studies of enzymes. Curr. Opin. Chem. Biol. 11, 182-187. https://doi.org/10.1016/j.cbpa.2007.01.684
  50. Shao, Y., Gan, Z., Epifanovsky, E., Gilbert, A.T.B., Wormit, M., Kussmann, J., Lange, A.W., Behn, A., Deng, J., Feng, X., et al. (2015). Advances in molecular quantum chemistry contained in the Q-Chem 4 program package. Mol. Phys. 113, 184-215. https://doi.org/10.1080/00268976.2014.952696
  51. Slonimskiy, Y.B., Muzzopappa, F., Maksimov, E.G., Wilson, A., Friedrich, T., Kirilovsky, D., and Sluchanko, N.N. (2019). Light-controlled carotenoid transfer between water-soluble proteins related to cyanobacterial photoprotection. FEBS J. 286, 1908-1924. https://doi.org/10.1111/febs.14803
  52. Sluchanko, N.N., Slonimskiy, Y.B., and Maksimov, E.G. (2017). Features of protein-protein interactions in the cyanobacterial photoprotection mechanism. Biochemistry (Mosc.) 82, 1592-1614. https://doi.org/10.1134/S000629791713003X
  53. Spezia, R., Knecht, S., and Mennucci, B. (2017). Excited state characterization of carbonyl containing carotenoids: a comparison between single and multireference descriptions. Phys. Chem. Chem. Phys. 19, 17156-17166. https://doi.org/10.1039/C7CP02941A
  54. Wang, J., Wang, W., Kollman, P.A., and Case, D.A. (2006). Automatic atom type and bond type perception in molecular mechanical calculations. J. Mol. Graph. Model. 25, 247-260. https://doi.org/10.1016/j.jmgm.2005.12.005
  55. Warshel, A. and Levitt, M. (1976). Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J. Mol. Biol. 103, 227-249. https://doi.org/10.1016/0022-2836(76)90311-9
  56. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M., and Barton, G.J. (2009). Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191. https://doi.org/10.1093/bioinformatics/btp033
  57. Wilson, A., Gwizdala, M., Mezzetti, A., Alexandre, M., Kerfeld, C.A., and Kirilovsky, D. (2012). The essential role of the N-terminal domain of the orange carotenoid protein in cyanobacterial photoprotection: importance of a positive charge for phycobilisome binding. Plant Cell 24, 1972-1983. https://doi.org/10.1105/tpc.112.096909
  58. Wilson, A., Kinney, J.N., Zwart, P.H., Punginelli, C., D'Haene, S., Perreau, F., Klein, M.G., Kirilovsky, D., and Kerfeld, C.A. (2010). Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J. Biol. Chem. 285, 18364-18375. https://doi.org/10.1074/jbc.M110.115709
  59. Wilson, A., Punginelli, C., Couturier, M., Perreau, F., and Kirilovsky, D. (2011). Essential role of two tyrosines and two tryptophans on the photoprotection activity of the orange carotenoid protein. Biochim. Biophys. Acta 1807, 293-301. https://doi.org/10.1016/j.bbabio.2010.12.009
  60. Yanai, T., Tew, D.P., and Handy, N.C. (2004). A new hybrid exchange-correlation functional using the coulomb-attenuating method (CAMB3LYP). Chem. Phys. Lett. 393, 51-57. https://doi.org/10.1016/j.cplett.2004.06.011
  61. Yang, H.W., Song, J.Y., Cho, S.M., Kwon, H.C., Pan, C.H., and Park, Y.I. (2020). Genomic survey of salt acclimation-related genes in the halophilic cyanobacterium Euhalothece sp. Z-M001. Sci. Rep. 10, 676.
  62. Zheng, L., Migliore, A., and Beratan, D.N. (2020). Electrostatic field-induced oscillator strength focusing in molecules. J. Phys. Chem. B 124, 6376-6388.  https://doi.org/10.1021/acs.jpcb.0c04783