Citation: Yu Mohan, Cheng Yuanyuan, Liu Yajun. Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence[J]. Acta Chimica Sinica, ;2020, 78(9): 989-993. doi: 10.6023/A20060269 shu

Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence

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

Corresponding author: Liu Yajun, yajun.liu@bnu.edu.cn
Received Date: 25 June 2020
Available Online: 15 July 2020
Fund Project: Project supported by the National Natural Science Foundation of China (Nos. 21673020, 21973005, 21421003)the National Natural Science Foundation of China 21973005the National Natural Science Foundation of China 21421003the National Natural Science Foundation of China 21673020

Figures(4)

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.
- luciferin,
- oxygenation,
- mechanism,
- single electron transfer,
- density functional theory
1. [1]
  Chen, F.; Liu, S.; Duan, X. Acta Chim. Sinica 2013, 71, 1035(in Chinese).
2. [2]
  Wilson, T.; Hastings, J. W. Annu. Rev. Cell. Dev. Bi. 1998, 14, 197. doi: 10.1146/annurev.cellbio.14.1.197
3. [3]
  Haddock, S. H. D.; Moline, M. A.; Case, J. F. Annu. Rev. Mar. Sci. 2010, 2, 443. doi: 10.1146/annurev-marine-120308-081028
4. [4]
  Lee, J. Bioluminescence, the Nature of the Light, University of Georgia, 2020, pp. 102~114.
5. [5]
  Ando, Y.; Niwa, K.; Yamada, N.; Enomot, T.; Irie, T.; Kubota, H.; Ohmiya, Y.; Akiyama, H. Nat. Photonics 2008, 2, 44. doi: 10.1038/nphoton.2007.251
6. [6]
  Wood, K. V. Photochem. Photobiol. 1995, 62, 662. doi: 10.1111/j.1751-1097.1995.tb08714.x
7. [7]
  Ugarova, N. N.; Brovko, L. Y. Luminescence 2002, 17, 321. doi: 10.1002/bio.688
8. [8]
  Schmidt, S. P.; Schuster, G. B. J. Am. Chem. Soc. 1978, 100, 1966. doi: 10.1021/ja00474a074
9. [9]
  Day, J. C.; Tisi, L. C.; Bailey, M. J. Luminescence 2004, 19, 8. doi: 10.1002/bio.749
10. [10]
  Navizet, I.; Liu, Y.-J.; Ferre, N.; Xiao, H.-Y.; Fang, W.-H.; Lindh, R. J. Am. Chem. Soc. 2010, 132, 706. doi: 10.1021/ja908051h
11. [11]
  Orlova, G.; Goddard, J. D.; Brovko, L. Y. J. Am. Chem. Soc. 2003, 125, 6962. doi: 10.1021/ja021255a
12. [12]
  Wilsey, S.; Bernardi, F.; Olivucci, M.; Robb, M. A.; Murphy, S.; Adam, W. J. Phys. Chem. A 1999, 103, 1669. doi: 10.1021/jp9848086
13. [13]
  Min, C.; Li, Z.; Cui, X.; Yang, X.; Huang, S.; Wang, S.; Ren, A. Chin. J. Org. Chem. 2015, 35, 432(in Chinese).
14. [14]
  Yue, L.; Liu, Y.-J.; Fang, W.-H. J. Am. Chem. Soc. 2012, 134, 11632. doi: 10.1021/ja302979t
15. [15]
  Yue, L.; Lan, Z.; Liu, Y.-J. J. Phys. Chem. Lett. 2015, 6, 540. doi: 10.1021/jz502305g
16. [16]
  Cheng, Y.-Y.; Liu, Y.-J. ChemPhysChem 2019, 20, 1720.
17. [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. doi: 10.1021/ja2041496
18. [18]
  Marahiel, M. A.; Stachelhaus, T.; Mootz, H. D. Chem. Rev. 1997, 97, 2651. doi: 10.1021/cr960029e
19. [19]
  Westheimer, F. H. Science 1987, 235, 1173. doi: 10.1126/science.2434996
20. [20]
  Barrozo, A.; Blaha-Nelson, D.; Williams, N. H.; Kamerlin, S. C. L. Pure Appl. Chem. 2017, 89, 715. doi: 10.1515/pac-2016-1125
21. [21]
  Duarte, F.; qvist, J.; Williams, N. H.; Kamerlin, S. C. L. J. Am. Chem. Soc. 2015, 137, 1081. doi: 10.1021/ja5082712
22. [22]
  Duarte, F.; Barrozo, A.; qvist, J.; Williams, N. H.; Kamerlin, S. C. L. J. Am. Chem. Soc. 2016, 138, 10664. doi: 10.1021/jacs.6b06277
23. [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. [24]
  Koo, J.-Y.; Schuster, G. B. J. Am. Chem. Soc. 1977, 99, 6107. doi: 10.1021/ja00460a050
25. [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. doi: 10.1021/jacs.5b03820
26. [26]
  Berraud-Pache, R.; Lindh, R.; Navizet, I. J. Phys. Chem. B 2018, 122, 5173. doi: 10.1021/acs.jpcb.8b00642
27. [27]
  Hirano, T.; Hasumi, Y.; Ohtsuka, K.; Maki, S.; Niwa, H.; Yamaji, M.; Hashizume, D. J. Am. Chem. Soc. 2009, 131, 2385. doi: 10.1021/ja808836b
28. [28]
  Shimomura, O. In Bioluminescence:Chemical Principles and Methods, World Scientific Publishing Co. Pte. Ltd., Singapore, 2006.
29. [29]
  Ding, B. W.; Liu, Y. J. J. Am. Chem. Soc. 2017, 139, 1106. doi: 10.1021/jacs.6b09119
30. [30]
  Luo, Y.; Liu, Y.-J. J. Phys. Chem. A 2019, 123, 4354. doi: 10.1021/acs.jpca.9b02084
31. [31]
  Zhao, Y.; Truhlar, D. G. Theor. Chem. Acc. 2007, 120, 215.
32. [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. [33]
  Dreuw, A.; Head-Gordon, M. Chem. Rev. 2005, 105, 4009. doi: 10.1021/cr0505627
34. [34]
  Boggio-Pasqua, M.; Heully, J.-L. Theor. Chem. Acc. 2015, 135, 9.
35. [35]
  Ess, D. H.; Cook, T. C. J. Phys. Chem. A 2012, 116, 4922. doi: 10.1021/jp300633j
36. [36]
  Gilson, M. K.; Honig, B. H. Biopolymers 1986, 25, 2097. doi: 10.1002/bip.360251106
37. [37]
  Pitera, J. W.; Falta, M.; van Gunsteren, W. F. Biophys. J. 2001, 80, 2546. doi: 10.1016/S0006-3495(01)76226-1
38. [38]
  Cossi, M.; Rega, N.; Scalmani, G.; Barone, V. J. Comput. Chem. 2003, 24, 669. doi: 10.1002/jcc.10189
39. [39]
  Nakatani, N.; Hasegawa, J.-y.; Nakatsuji, H. J. Am. Chem. Soc. 2007, 129, 8756. doi: 10.1021/ja0611691
40. [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.
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