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.
1. [1]
  Jie ZHAO , Sen LIU , Qikang YIN , Xiaoqing LU , Zhaojie WANG . Theoretical calculation of selective adsorption and separation of CO₂ by alkali metal modified naphthalene/naphthalenediyne. Chinese Journal of Inorganic Chemistry, 2024, 40(3): 515-522. doi: 10.11862/CJIC.20230385
2. [2]
  Maitri Bhattacharjee , Rekha Boruah Smriti , R. N. Dutta Purkayastha , Waldemar Maniukiewicz , Shubhamoy Chowdhury , Debasish Maiti , Tamanna Akhtar . Synthesis, structural characterization, bio-activity, and density functional theory calculation on Cu(Ⅱ) complexes with hydrazone-based Schiff base ligands. Chinese Journal of Inorganic Chemistry, 2024, 40(7): 1409-1422. doi: 10.11862/CJIC.20240007
3. [3]
  Chunmei GUO , Weihan YIN , Jingyi SHI , Jianhang ZHAO , Ying CHEN , Quli FAN . Facile construction and peroxidase-like activity of single-atom platinum nanozyme. Chinese Journal of Inorganic Chemistry, 2024, 40(9): 1633-1639. doi: 10.11862/CJIC.20240162
4. [4]
  Xiaosong PU , Hangkai WU , Taohong LI , Huijuan LI , Shouqing LIU , Yuanbo HUANG , Xuemei LI . Adsorption performance and removal mechanism of Cd(Ⅱ) in water by magnesium modified carbon foam. Chinese Journal of Inorganic Chemistry, 2024, 40(8): 1537-1548. doi: 10.11862/CJIC.20240030
5. [5]
  Yonghui ZHOU , Rujun HUANG , Dongchao YAO , Aiwei ZHANG , Yuhang SUN , Zhujun CHEN , Baisong ZHU , Youxuan ZHENG . Synthesis and photoelectric properties of fluorescence materials with electron donor-acceptor structures based on quinoxaline and pyridinopyrazine, carbazole, and diphenylamine derivatives. Chinese Journal of Inorganic Chemistry, 2024, 40(4): 701-712. doi: 10.11862/CJIC.20230373
6. [6]
  Chuanming GUO , Kaiyang ZHANG , Yun WU , Rui YAO , Qiang ZHAO , Jinping LI , Guang LIU . Performance of MnO₂-0.39IrO_x composite oxides for water oxidation reaction in acidic media. Chinese Journal of Inorganic Chemistry, 2024, 40(6): 1135-1142. doi: 10.11862/CJIC.20230459
7. [7]
  Zhihuan XU , Qing KANG , Yuzhen LONG , Qian YUAN , Cidong LIU , Xin LI , Genghuai TANG , Yuqing LIAO . Effect of graphene oxide concentration on the electrochemical properties of reduced graphene oxide/ZnS. Chinese Journal of Inorganic Chemistry, 2024, 40(7): 1329-1336. doi: 10.11862/CJIC.20230447
8. [8]
  Yingchun ZHANG , Yiwei SHI , Ruijie YANG , Xin WANG , Zhiguo SONG , Min WANG . Dual ligands manganese complexes based on benzene sulfonic acid and 2, 2′-bipyridine: Structure and catalytic properties and mechanism in Mannich reaction. Chinese Journal of Inorganic Chemistry, 2024, 40(8): 1501-1510. doi: 10.11862/CJIC.20240078
9. [9]
  Kai CHEN , Fengshun WU , Shun XIAO , Jinbao ZHANG , Lihua ZHU . PtRu/nitrogen-doped carbon for electrocatalytic methanol oxidation and hydrogen evolution by water electrolysis. Chinese Journal of Inorganic Chemistry, 2024, 40(7): 1357-1367. doi: 10.11862/CJIC.20230350
10. [10]
  Zhuo WANG , Junshan ZHANG , Shaoyan YANG , Lingyan ZHOU , Yedi LI , Yuanpei LAN . Preparation and photocatalytic performance of CeO₂-reduced graphene oxide by thermal decomposition. Chinese Journal of Inorganic Chemistry, 2024, 40(9): 1708-1718. doi: 10.11862/CJIC.20240067
11. [11]
  Zhanggui DUAN , Yi PEI , Shanshan ZHENG , Zhaoyang WANG , Yongguang WANG , Junjie WANG , Yang HU , Chunxin LÜ , Wei ZHONG . Preparation of UiO-66-NH₂ supported copper catalyst and its catalytic activity on alcohol oxidation. Chinese Journal of Inorganic Chemistry, 2024, 40(3): 496-506. doi: 10.11862/CJIC.20230317
12. [12]
  Bo YANG , Gongxuan LÜ , Jiantai MA . Nickel phosphide modified phosphorus doped gallium oxide for visible light photocatalytic water splitting to hydrogen. Chinese Journal of Inorganic Chemistry, 2024, 40(4): 736-750. doi: 10.11862/CJIC.20230346
13. [13]
  Zeyu XU , Anlei DANG , Bihua DENG , Xiaoxin ZUO , Yu LU , Ping YANG , Wenzhu YIN . Evaluation of the efficacy of graphene oxide quantum dots as an ovalbumin delivery platform and adjuvant for immune enhancement. Chinese Journal of Inorganic Chemistry, 2024, 40(6): 1065-1078. doi: 10.11862/CJIC.20240099
14. [14]
  Siyu HOU , Weiyao LI , Jiadong LIU , Fei WANG , Wensi LIU , Jing YANG , Ying ZHANG . Preparation and catalytic performance of magnetic nano iron oxide by oxidation co-precipitation method. Chinese Journal of Inorganic Chemistry, 2024, 40(8): 1577-1582. doi: 10.11862/CJIC.20230469
15. [15]
  Xiaoning TANG , Shu XIA , Jie LEI , Xingfu YANG , Qiuyang LUO , Junnan LIU , An XUE . Fluorine-doped MnO₂ with oxygen vacancy for stabilizing Zn-ion batteries. Chinese Journal of Inorganic Chemistry, 2024, 40(9): 1671-1678. doi: 10.11862/CJIC.20240149
16. [16]
  Endong YANG , Haoze TIAN , Ke ZHANG , Yongbing LOU . Efficient oxygen evolution reaction of CuCo₂O₄/NiFe-layered bimetallic hydroxide core-shell nanoflower sphere arrays. Chinese Journal of Inorganic Chemistry, 2024, 40(5): 930-940. doi: 10.11862/CJIC.20230369
17. [17]
  Yan LIU , Jiaxin GUO , Song YANG , Shixian XU , Yanyan YANG , Zhongliang YU , Xiaogang HAO . Exclusionary recovery of phosphate anions with low concentration from wastewater using a CoNi-layered double hydroxide/graphene electronically controlled separation film. Chinese Journal of Inorganic Chemistry, 2024, 40(9): 1775-1783. doi: 10.11862/CJIC.20240043
18. [18]
  Xiaoning TANG , Junnan LIU , Xingfu YANG , Jie LEI , Qiuyang LUO , Shu XIA , An XUE . Effect of sodium alginate-sodium carboxymethylcellulose gel layer on the stability of Zn anodes. Chinese Journal of Inorganic Chemistry, 2024, 40(8): 1452-1460. doi: 10.11862/CJIC.20240191
19. [19]
  Siyi ZHONG , Xiaowen LIN , Jiaxin LIU , Ruyi WANG , Tao LIANG , Zhengfeng DENG , Ao ZHONG , Cuiping HAN . Targeting imaging and detection of ovarian cancer cells based on fluorescent magnetic carbon dots. Chinese Journal of Inorganic Chemistry, 2024, 40(8): 1483-1490. doi: 10.11862/CJIC.20240093
20. [20]
  Peiran ZHAO , Yuqian LIU , Cheng HE , Chunying DUAN . A functionalized Eu³⁺ metal-organic framework for selective fluorescent detection of pyrene. Chinese Journal of Inorganic Chemistry, 2024, 40(4): 713-724. doi: 10.11862/CJIC.20230355

Get Citation

PDF

XML

Metrics

PDF Downloads(26)
Abstract views(2960)
HTML views(570)

通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142