Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence

doi:10.6023/A20060269

Acta Chimica Sinica ›› 2020, Vol. 78 ›› Issue (9): 989-993.DOI: 10.6023/A20060269 Previous Articles Next Articles

Article

萤火虫生物发光中加氧反应机理的理论研究

于沫涵^a, 程媛媛^b, 刘亚军^a

a 北京师范大学化学学院理论及计算光化学教育部重点实验室北京 100875;
b 东华理工大学江西省质谱科学与仪器重点实验室南昌 330013

投稿日期:2020-06-25 发布日期:2020-07-17
通讯作者: 刘亚军 E-mail:yajun.liu@bnu.edu.cn
基金资助:
项目受国家自然科学基金（Nos.21673020，21973005，21421003）资助.

Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence

Yu Mohan^a, Cheng Yuanyuan^b, Liu Yajun^a

a Key Laboratory of Theoretical and Computational Photochemistry, Ministry of Education, College of Chemistry, Beijing Normal University, Beijing 100875, China;
b Jiangxi Key Laboratory for Mass Spectrometry and Instrumentation, East China University of Technology, Nanchang 330013, China

Received:2020-06-25 Published:2020-07-17
Supported by:
Project supported by the National Natural Science Foundation of China (Nos. 21673020, 21973005, 21421003).

1. A20060269.pdf(1014KB)

Abstract

As the most common bioluminescence (BL), firefly BL, is of great significance in the fields of biotechnology, biomedicine and so on. The entire BL process involves a series of complicate in vivo chemical reactions. The BL is initiated by the enzymatic oxidation of luciferin. This is a spin-forbidden reaction of low efficiency, because that luciferin is in singlet state and O₂ is in triplet state. However, firefly is till-now the most efficient system of converting chemical energy to light energy. Why this spin-forbidden reaction occurs efficiently? A single electron transfer (SET) mechanism has been confirmed on this reaction by experiments. However, there is lack of a complete and detailed description of the mechanism and reaction process. Via a calculation of density functional theory (DFT), this article described the complete process of this reaction. The oxygenation of luciferin is initiated by a SET from singlet L^3- to triplet O₂ to form RC ³[L^·2-…O₂^·-]. Then the reaction is carried out on the potential energy surface (PES) of triplet state (T₁), on which O₂^·- performs a nucleophilic attack on C4 of L^·2-. There is an intersystem crossing between the ground (S₀) and T₁ PESs nearby the first transition state (TS1). After the ISC (intersystem crossing), the reaction continuously undergoes on the S₀ PES to produce dioxetanone FDO^- via two TSs and two intermediates (Ints). The analysis on electron densities and natural orbitals indicates that there is a quick reaction of biradical annihilation around the ISC. About 11.9 kcal·mol^-1 energy is needed to reach the ISC before the whole reaction occurs on the S₀ PES. The highest barrier of the reactions on the S₀ PES is only 4.2 kcal·mol^-1. The biradical annihilation around the ISC and the very low energy barriers explain the reason of the spin-forbidden reaction with high efficiency. This study is helpful for understanding the initiation of firefly BL and the other oxygen-dependent BL.

Key words: luciferin, oxygenation, mechanism, single electron transfer, density functional theory

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Yu Mohan, Cheng Yuanyuan, Liu Yajun. Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence[J]. Acta Chimica Sinica, 2020, 78(9): 989-993.

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[1] Chen, F.; Liu, S.; Duan, X. Acta Chim. Sinica 2013, 71, 1035(in Chinese). (陈浮, 刘树深, 段欣甜, 化学学报, 2013, 71, 1035.)
[2] Wilson, T.; Hastings, J. W. Annu. Rev. Cell. Dev. Bi. 1998, 14, 197.
[3] Haddock, S. H. D.; Moline, M. A.; Case, J. F. Annu. Rev. Mar. Sci. 2010, 2, 443.
[4] Lee, J. Bioluminescence, the Nature of the Light, University of Georgia, 2020, pp. 102~114.
[5] Ando, Y.; Niwa, K.; Yamada, N.; Enomot, T.; Irie, T.; Kubota, H.; Ohmiya, Y.; Akiyama, H. Nat. Photonics 2008, 2, 44.
[6] Wood, K. V. Photochem. Photobiol. 1995, 62, 662.
[7] Ugarova, N. N.; Brovko, L. Y. Luminescence 2002, 17, 321.
[8] Schmidt, S. P.; Schuster, G. B. J. Am. Chem. Soc. 1978, 100, 1966.
[9] Day, J. C.; Tisi, L. C.; Bailey, M. J. Luminescence 2004, 19, 8.
[10] Navizet, I.; Liu, Y.-J.; Ferre, N.; Xiao, H.-Y.; Fang, W.-H.; Lindh, R. J. Am. Chem. Soc. 2010, 132, 706.
[11] Orlova, G.; Goddard, J. D.; Brovko, L. Y. J. Am. Chem. Soc. 2003, 125, 6962.
[12] Wilsey, S.; Bernardi, F.; Olivucci, M.; Robb, M. A.; Murphy, S.; Adam, W. J. Phys. Chem. A 1999, 103, 1669.
[13] Min, C.; Li, Z.; Cui, X.; Yang, X.; Huang, S.; Wang, S.; Ren, A. Chin. J. Org. Chem. 2015, 35, 432(in Chinese). (闵春刚, 李作盛, 崔小英, 杨喜昆, 黄绍军, 王绍华, 任爱民, 有机化学, 2015, 35, 432.)
[14] Yue, L.; Liu, Y.-J.; Fang, W.-H. J. Am. Chem. Soc. 2012, 134, 11632.
[15] Yue, L.; Lan, Z.; Liu, Y.-J. J. Phys. Chem. Lett. 2015, 6, 540.
[16] Cheng, Y.-Y.; Liu, Y.-J. ChemPhysChem 2019, 20, 1720.
[17] Branching, B. R.; Rosenberg, J. C.; Fontaine, D. M.; Southworth, T. L.; Behney, C. E.; Uzasci, L. J. Am. Chem. Soc. 2011, 133, 11088.
[18] Marahiel, M. A.; Stachelhaus, T.; Mootz, H. D. Chem. Rev. 1997, 97, 2651.
[19] Westheimer, F. H. Science 1987, 235, 1173.
[20] Barrozo, A.; Blaha-Nelson, D.; Williams, N. H.; Kamerlin, S. C. L. Pure Appl. Chem. 2017, 89, 715.
[21] Duarte, F.; Åqvist, J.; Williams, N. H.; Kamerlin, S. C. L. J. Am. Chem. Soc. 2015, 137, 1081.
[22] Duarte, F.; Barrozo, A.; Åqvist, J.; Williams, N. H.; Kamerlin, S. C. L. J. Am. Chem. Soc. 2016, 138, 10664.
[23] Nelson, D. L.; Cox, M. M. Lehninger Principles of Biochemistry, 7th ed., W. H. Freeman and Company, New York, 2013, pp. 1370~1380.
[24] Koo, J.-Y.; Schuster, G. B. J. Am. Chem. Soc. 1977, 99, 6107.
[25] Branchini, B. R.; Behney, C. E.; Southworth, T. L.; Fontaine, D. M.; Gulick, A. M.; Vinyard, D. J.; Brudvig, G. W. J. Am. Chem. Soc. 2015, 137, 7592.
[26] Berraud-Pache, R.; Lindh, R.; Navizet, I. J. Phys. Chem. B 2018, 122, 5173.
[27] Hirano, T.; Hasumi, Y.; Ohtsuka, K.; Maki, S.; Niwa, H.; Yamaji, M.; Hashizume, D. J. Am. Chem. Soc. 2009, 131, 2385.
[28] Shimomura, O. In Bioluminescence:Chemical Principles and Methods, World Scientific Publishing Co. Pte. Ltd., Singapore, 2006.
[29] Ding, B. W.; Liu, Y. J. J. Am. Chem. Soc. 2017, 139, 1106.
[30] Luo, Y.; Liu, Y.-J. J. Phys. Chem. A 2019, 123, 4354.
[31] Zhao, Y.; Truhlar, D. G. Theor. Chem. Acc. 2007, 120, 215.
[32] Perdew, J. P.; Ruzsinszky, A.; Tao, J. M.; Staroverov, V. N.; Scuseria, G. E.; Csonka, G. I. J. Chem. Phys. 2005, 123, A1133.
[33] Dreuw, A.; Head-Gordon, M. Chem. Rev. 2005, 105, 4009.
[34] Boggio-Pasqua, M.; Heully, J.-L. Theor. Chem. Acc. 2015, 135, 9.
[35] Ess, D. H.; Cook, T. C. J. Phys. Chem. A 2012, 116, 4922.
[36] Gilson, M. K.; Honig, B. H. Biopolymers 1986, 25, 2097.
[37] Pitera, J. W.; Falta, M.; van Gunsteren, W. F. Biophys. J. 2001, 80, 2546.
[38] Cossi, M.; Rega, N.; Scalmani, G.; Barone, V. J. Comput. Chem. 2003, 24, 669.
[39] Nakatani, N.; Hasegawa, J.-y.; Nakatsuji, H. J. Am. Chem. Soc. 2007, 129, 8756.
[40] 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.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, J. J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Keith, T.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, J. M.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, O.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, Revision D. Gaussian Inc., Wallingford, 2009.

萤火虫生物发光中加氧反应机理的理论研究

Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence

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