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Computational Bioluminescence
Yi-Qi Tang,
Ya-Jun Liu,
Yi-Qi Tang
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorCorresponding Author
Ya-Jun Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
E-mail: [email protected]Search for more papers by this authorYi-Qi Tang,
Ya-Jun Liu,
Yi-Qi Tang
College of Chemistry, Beijing Normal University, Beijing, 100875 China
Search for more papers by this authorCorresponding Author
Ya-Jun Liu
College of Chemistry, Beijing Normal University, Beijing, 100875 China
E-mail: [email protected]Search for more papers by this authorAbstract
Bioluminescence (BL) is an amazing natural phenomenon whose visible light is produced by living organisms. Due to its high sensitivity, high selectivity and high signal-to-noise ratio, BL has been applied broadly in biotechnology and biomedical fields. However, for centuries, we can only receive some sporadic and static information from experimental observations, the mechanism of most BL is unknown. In the past 14 years, we have been performing theoretical study on all kinds of bioluminescent systems, and have uncovered the mechanism and details of several BLs. Here as an example, we qualitatively introduce our theoretical study of firefly BL in this account.
References
- 1
Wiedeman, E. Ann. Mys. Chem. 1888, 34, 446.
10.1002/andp.18882700703 Google Scholar
- 2
Shimomura, O. Bioluminescence,
Chemical Principles and Methods, World Scientific, Singapore, 2006.
10.1142/6102 Google Scholar
- 3 Harvey, E. N. A History of Luminescence from the Earliest Times until 1900, American Philosophical Society, Philadelphia, 1989.
- 4 Campbell, A. K. Chemiluminescence: Principles and Applications in Biology and Medicine, Ellis Horwood, Chichester, 1988.
- 5
Roda, A. In Chemiluminescence and Bioluminescence: Past, Present and Future, Ed.: A. Roda, Royal Society of Chemistry, Cambridge, 2010.
10.1039/9781849732024 Google Scholar
- 6 Harvey, E. N. On the Chemical Nature of the Luminous Material of the Firefly. Science (New York, NY) 1914, 40, 33–34.
- 7 Subach, F. V.; Verkhusha, V. V. Chromophore Transformations in Red Fluorescent Proteins. Chem. Rev. 2012, 112, 4308–4327.
- 8 Vacher, M.; Fdez Galván, I.; Ding, B. W.; Schramm, S.; Berraud-Pache, R.; Naumov, P.; Ferré, N.; Liu, Y. J.; Navizet, I.; Roca-Sanjuán, D.; Baader, W. J.; Lindh, R. Chemi- and Bioluminescence of Cyclic Peroxides. Chem. Rev. 2018, 118, 6927–6974.
- 9 Maltsev, O. V.; Nath, N. K.; Naumov, P.; Hintermann, L. Why is Firefly Oxyluciferin a Notoriously Labile Substance? Angew. Chem. Int. Ed. 2014, 53, 847–850.
- 10 Murakami, M.; Kouyama, T. Crystal Structure of Squid Rhodopsin. Nature 2008, 453, 363–367.
- 11 McCutcheon, D. C.; Paley, M. A.; Steinhardt, R. C.; Prescher, J. A. Expedient Synthesis of Electronically Modified Luciferins for Bioluminescence Imaging. J. Am. Chem. Soc. 2012, 134, 7604–7607.
- 12 Branchini, B. R.; Rosenberg, J. C.; Fontaine, D. M.; Southworth, T. L.; Behney, C. E.; Uzasci, L. Bioluminescence Is Produced from a Trapped Firefly Luciferase Conformation Predicted by the Domain Alternation Mechanism. J. Am. Chem. Soc. 2011, 133, 11088–11091.
- 13 Sun, X.; Zhao, Y.; Lin, V. S.; Slowing, I. I.; Trewyn, B. G. Luciferase and Luciferin Co-immobilized Mesoporous Silica Nanoparticle Materials for Intracellular Biocatalysis. J. Am. Chem. Soc. 2011, 133, 18554–18557.
- 14 Wu, C.; Mino, K.; Akimoto, H.; Kawabata, M.; Nakamura, K.; Ozaki, M.; Ohmiya, Y. In Vivo Far-Red Luminescence Imaging of a Biomarker Based on BRET from Cypridina Bioluminescence to an Organic Dye. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 15599–15603.
- 15 Wu, J.; Tokuyama, S.; Nagai, K.; Yasuda, N.; Noguchi, K.; Matsumoto, T.; Hirai, H.; Kawagishi, H. Strophasterols A to D with an Unprecedented Steroid Skeleton: from the Mushroom Stropharia rugosoannulata. Angew. Chem. Int. Ed. 2012, 51, 10820–10822.
- 16 Liu, Z. J.; Stepanyuk, G. A.; Vysotski, E. S.; Lee, J.; Markova, S. V.; Malikova, N. P.; Wang, B. C. Crystal Structure of Obelin after Ca2+-Triggered Bioluminescence Suggests Neutral Coelenteramide as the Primary Excited State. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 2570–2575.
- 17 Campbell, Z. T.; Weichsel, A.; Montfort, W. R.; Baldwin, T. O. Crystal Structure of the Bacterial Luciferase/Flavin Complex Provides Insight into the Function of the β Subunit. Biochemistry 2009, 48, 6085–6094.
- 18 Schultz, L. W.; Liu, L.; Cegielski, M.; Hastings, J. W. Crystal Structure of a pH-Regulated Luciferase Catalyzing the Bioluminescent Oxidation of an Open Tetrapyrrole. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 1378–1383.
- 19 Ohmiya, Y.; Kojima, S.; Nakamura, M.; Niwa, H. Bioluminescence in the Limpet-Like Snail, Latia neritoides. Bull. Chem. Soc. Jpn. 2005, 78, 1197–1205.
- 20 Vysotski, E. S.; Liu, Z.-J.; Markova, S. V.; Blinks, J. R.; Deng, L.; Frank, L. A.; Herko, M.; Malikova, N. P.; Rose, J. P.; Wang, B.-C.; Lee, J. Violet Bioluminescence and Fast Kinetics from W92F Obelin: Structure- Based Proposals for the Bioluminescence Triggering and the Identification of the Emitting Species. Biochemistry 2003, 42, 6013–6024.
- 21 Rota, E.; Zalesskaja, N. T.; Rodionova, N. S.; Petushkov, V. N. Redescription of Fridericia heliota (Annelida, Clitellata: Enchytraeidae), a Luminous Worm from the Siberian Taiga, with a Review of Bioluminescence in the Oligochaeta. J. Zool., Lond. 2003, 260, 291–299.
- 22 Lorenz, W. W.; Mccann, R. O.; Longiaru, M.; Cormier, M. J. Isolation and Expression of a cDNA Encoding Renilla reniformis Luciferase. Proc. Natl. Acad. Sci. U. S. A. 1991, 88, 4438–4442.
- 23 Hirano, T.; Takahashi, Y.; Kondo, H.; Maki, S.; Kojima, S.; Ikeda, H.; Niwa, H. The Reaction Mechanism for the High Quantum Yield of Cypridina (Vargula) Bioluminescence Supported by the Chemiluminescence of 6-Aryl-2-Methylimidazo[1,2-a]Pyrazin-3(7H)-Ones (Cypridina Luciferin Analogues). Photochem. Photobiol. Sci. 2008, 7, 197–207.
- 24 Chen, S.-F.; Liu, Y.-J.; Navizet, I.; Ferré, N.; Fang, W.-H.; Lindh, R. Systematic Theoretical Investigation on the Light Emitter of Firefly. J. Chem. Theory Comput. 2011, 7, 798–803.
- 25 Cheng, Y.-Y.; Liu, Y.-J. Vibrationally Resolved Absorption and Fluorescence Spectra of Firefly Luciferin: A Theoretical Simulation in the Gas Phase and in Solution. Photochem. Photobiol. 2016, 92, 552–560.
- 26 Cheng, Y.-Y.; Zhu, J.; Liu, Y.-J. Theoretical Tuning of the Firefly Bioluminescence Spectra by the Modification of Oxyluciferin. Chem. Phys. Lett. 2014, 591, 156–160.
- 27 Liu, F.; Liu, Y.; Vico, L. D.; Lindh, R. Theoretical Study of the Chemiluminescent Decomposition of Dioxetanone. J. Am. Chem. Soc. 2009, 131, 6181–6188.
- 28 Liu, Y.; Fang, W. Ab Initio Investigation on the Structures and Spectra of the Firefly Luciferin. Sci. China, Ser. B 2007, 50, 725–730.
- 29 Liu, Y.-J.; Vico, L. D.; Lindh, R. Ab Initio Investigation on the Chemical Origin of the Firefly Bioluminescence. J. Photochem. Photobiol., A 2008, 194, 261–267.
- 30 Navizet, I.; Liu, Y.-J.; Ferré, N.; Xiao, H.-Y.; Fang, W.-H.; Lindh, R. Color-Tuning Mechanism of Firefly Investigated by Multi-Configurational Perturbation Method. J. Am. Chem. Soc. 2010, 132, 706–712.
- 31 Navizet, I.; Roca-Sanjuán, D.; Yue, L.; Liu, Y.-J.; Ferré, N.; Lindh, R. Are the Bio- and Chemiluminescence States of the Firefly Oxyluciferin the Same as the Fluorescence State? Photochem. Photobiol. 2013, 89, 319–325.
- 32 Yue, L.; Lan, Z.; Liu, Y.-J. The Theoretical Estimation of the Bioluminescent Efficiency of the Firefly via a Nonadiabatic Molecular Dynamics Simulation. J. Phys. Chem. Lett. 2015, 6, 540–548.
- 33 Yue, L.; Liu, Y.-J.; Fang, W.-H. Mechanistic Insight into the Chemiluminescent Decomposition of Firefly Dioxetanone. J. Am. Chem. Soc. 2012, 134, 11632–11639.
- 34 Roca-Sanjuán, D.; France's-Monerris, A.; Galván, I. F.; Farahani, P.; Lindh, R.; Liu, Y.-J. Advances in Computational Photochemistry and Chemiluminescence of Biological and Nanotechnological Molecules. In Photochemistry, Vol. 44, Eds.: A. Albini; E. Fasani, Royal Society of Chemistry, Cambridge, UK, 2017, pp. 16–60.
- 35 Cheng, Y.-Y.; Liu, Y.-J. Theoretical Development of Near-Infrared Bioluminescent Systems. Chem. Eur. J. 2018, 24, 9340–9352.
- 36 Cheng, Y.-Y.; Liu, Y.-J. Luciferin Regeneration in Firefly Bioluminescence via Proton-Transfer-Facilitated Hydrolysis, Condensation and Chiral Inversion. ChemPhysChem 2019, 20, 1719–1727.
- 37 Yu, M.; Liu, Y.-J. Same Luciferin in Different Luciferases Emitting Different-Color Light. A Theoretical Study on Beetle Bioluminescence. J. Chem. Theory Comput. 2020, 16, 3904–3909.
- 38 Ding, B.-W.; Naumov, P.; Liu, Y.-J. Mechanistic Insight into Marine Bioluminescence: Photochemistry of the Chemiexcited Cypridina (Sea Firefly) Lumophore. J. Chem. Theory Comput. 2015, 11, 591–599.
- 39 Naumov, P.; Wu, C.; Liu, Y.-J.; Ohmiya, Y. Spectrochemistry and Artificial Color Modulation of Cypridina Luminescence: Indirect Evidence for Chemiexcitation of a Neutral Dioxetanone and Emission from a Neutral Amide. Photochem. Photobiol. Sci. 2012, 11, 1151–1155.
- 40 Roca-Sanjuán, D.; Delcey, M. G.; Navizet, I.; Ferré, N.; Liu, Y.-J.; Lindh, R. Chemiluminescence and Fluorescence States of a Small Model for Coelenteramide and Cypridina Oxyluciferin: A CASSCF/CASPT2 Study. J. Chem. Theory Comput. 2011, 7, 4060–4069.
- 41 Chen, S.-F.; Ferré, N.; Liu, Y.-J. QM/MM Study on the Light Emitters of Aequorin Chemiluminescence, Bioluminescence, and Fluorescence: a General Understanding of the Bioluminescence of Several Marine Organisms. Chem. Eur. J. 2013, 19, 8466–8472.
- 42 Ding, B. W.; Eremeeva, E. V.; Vysotski, E. S.; Liu, Y. J. Luminescence Activity Decreases When v-coelenterazine Replaces Coelenterazine in Calcium-Regulated Photoprotein-A Theoretical and Experimental Study. Photochem. Photobiol. 2020, 96, 1047–1060.
- 43 Chen, S.; Navizet, I.; Lindh, R.; Liu, Y.; Ferré, N. Hybrid QM/MM Simulations of the Obelin Bioluminescence and Fluorescence Reveal an Unexpected Light Emitter. J. Phys. Chem. B 2014, 118, 2896–2903.
- 44 Gao, M.; Ding, B.-W.; Liu, Y.-J. Tuning the Fluorescence of Calcium- Discharged Photoprotein Obelin via Mutating at the His22-Phe88- Trp92 Triad - a QM/MM Study. Photochem. Photobiol. Sci. 2019, 18, 1823–1832.
- 45 Hou, C.; Liu, Y.-J.; Ferré, N.; Fang, W.-H. Understanding Bacterial Bioluminescence: a Theoretical Study of the Entire Process, from Reduced Flavin to Light Emission. Chem. Eur. J. 2014, 20, 7979–7986.
- 46 Luo, Y.; Liu, Y.-J. Bioluminophore and Flavin Mononucleotide Fluorescence Quenching of Bacterial Bioluminescence-A Theoretical Study. Chem. Eur. J. 2016, 22, 16243–16249.
- 47 Luo, Y.; Liu, Y.-J. Revisiting the Origin of Bacterial Bioluminescence: QM/MM Study on Oxygenation Reaction of Reduced Flavin in Protein. Chem. Phys. Chem. 2019, 20, 405–409.
- 48 Ding, B.-W.; Liu, Y.-J. Bioluminescence of Firefly Squid via Mechanism of Single Electron-Transfer Oxygenation and Charge-Transfer-Induced Luminescence. J. Am. Chem. Soc. 2017, 139, 1106–1119.
- 49 Wang, M.-Y.; Liu, Y.-J. Theoretical Study of Dinoflagellate Bioluminescence. Photochem. Photobiol. 2017, 93, 511–518.
- 50 Wang, M.-Y.; Liu, Y.-J. Mechanistic Insight into Initiation of Dinoflagellate Bioluminescence. J. Photochem. Photobiol., A 2020, 394, 112488.
- 51 Yu, M.; Ohmiya, Y.; Naumov, P.; Liu, Y.-J. Theoretical Insight into the Emission Properties of the Luciferin and Oxyluciferin of Latia. Photochem. Photobiol. 2018, 94, 540–544.
- 52 Tang, Y.-Q.; Liu, Y.-J. Theoretical Study on Bioluminescent Mechanism and Process of Siberian Luminous Earthworm Fridericia heliota. J. Photochem. Photobiol., A 2019, 380, 111870.
- 53 Lee, J. Bioluminescence, the Nature of Light, The University of Georgia, 2020.
- 54Scientists Investigate How Fireflies Emit Different Colors of Light. https://phys.org/news/2010–01-scientists-fireflies-emit.html.
- 55Flashes of Brilliance. https://www.biographic.com/posts/sto/flashes- of-brilliance.
- 56 Marahiel, M. A.; Stachelhaus, T.; Mootz, H. D. Modular Peptide Synthetases Involved in Nonribosomal Peptide Synthesis. Chem. Rev. 1997, 97, 2651–2673.
- 57 Westheimer, F. H. Why Nature Chose Phosphates. Science 1987, 235, 1173–1177.
- 58 Barrozo, A.; Blaha-Nelson, D.; Williams, N. H.; Kamerlin, S. C. L. The Effect of Magnesium Ions on Triphosphate Hydrolysis. Pure. Appl. Chem. 2017, 89, 715–727.
- 59 Duarte, F.; Aqvist, J.; Williams, N. H.; Kamerlin, S. C. Resolving Apparent Conflicts between Theoretical and Experimental Models of Phosphate Monoester Hydrolysis. J. Am. Chem. Soc. 2015, 137, 1081–1093.
- 60 Duarte, F.; Barrozo, A.; Åqvist, J.; Williams, N. H.; Kamerlin, S. C. L. The Competing Mechanisms of Phosphate Monoester Dianion Hydrolysis. J. Am. Chem. Soc. 2016, 138, 10664–10673.
- 61 Ando, Y.; Niwa, K.; Yamada, N.; Enomoto, T.; Irie, T.; Kubota, H.; Ohmiya, Y.; Akiyama, H. Firefly Bioluminescence Quantum Yield and Colour Change by pH-Sensitive Green Emission. Nat. Photonics 2007, 2, 44–47.
- 62 Yu, M.; Cheng, Y.-Y.; Liu, Y.-J. Mechanistic Study of Oxygenation Reaction in Firefly Bioluminescence. Acta Chim. Sinica 2020, 78, 989–993.
- 63 Cheng, Y. Y.; Liu, Y. J. What Exactly Is the Light Emitter of a Firefly? J. Chem. Theory Comput. 2015, 11, 5360–5370.
- 64 Pirrung, M. C.; Dorsey, A.; Howitt, N. D.; Liao, J. β-Deuterium Isotope Effects on Firefly Luciferase Bioluminescence. ChemistryOpen 2017, 6, 697–700.
- 65 Berraud-Pache, R.; Garcia-Iriepa, C.; Navizet, I. Modeling Chemical Reactions by QM/MM Calculations: The Case of the Tautomerization in Fireflies Bioluminescent Systems. Front. Chem. 2018, 6, 116.
- 66 Okada, K.; Iio, H.; Kubota, I.; Goto, T. Firefly Bioluminescence III. Conversion of Oxyluciferin to Luciferin in Firefly. Tetrahedron Lett. 1974, 32, 2771–2774.
