Effect of Viscous Media on the Quantum Yield of Bioluminescence in a Reaction Catalyzed by Bacterial Luciferase

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Abstract

Based on previously obtained data on the transient kinetics of the bioluminescent reaction catalyzed by P. leiognathi luciferase in media with polyols and sugars, the relative quantum yield of bioluminescence per substrate molecule was determined using mathematical modeling. It was found that in some media the relative quantum yield per aldehyde molecule increases compared to the value in the buffer: by 18% in the presence of glycerol and by 33% in the presence of sucrose. The conformation of the side chain of αHis44, which is the functionally important and conservative in all bacterial luciferases, was analyzed using molecular dynamics methods. It has been established that in the presence of all cosolvents there is an increase in the probability of formation the optimal for catalysis orientation of this amino acid, which may contribute to the observed increase in the quantum yield of bioluminescence in viscous media.

About the authors

A. E Lisitsa

Siberian Federal University

Email: ALisitsa@sfu-kras.ru
Krasnoyarsk, Russia

L. A Sukovatyi

Siberian Federal University

Krasnoyarsk, Russia

V. A Kratasyuk

Siberian Federal University; Institute of Biophysics, Federal Research Center “Krasnoyarsk Science Center” of the Siberian Branch of the Russian Academy of Sciences

Krasnoyarsk, Russia; Krasnoyarsk, Russia

E. V Nemtseva

Siberian Federal University; Institute of Biophysics, Federal Research Center “Krasnoyarsk Science Center” of the Siberian Branch of the Russian Academy of Sciences

Krasnoyarsk, Russia; Krasnoyarsk, Russia

References

  1. Lee J., Bioluminescence, the nature of the light (University of Georgia, 2020).
  2. Немцева Е. В. и Кудряшева Н. С. Механизм электронного возбуждения в биолюминесцентной реакции бактерий. Успехи химии, 76 (1), 101–112 (2007).
  3. Nakamura T. and Matsuda K. Studies on luciferase from Photobacterium phosphoreum. I. Purification and physicochemical properties. J. Biochem., 70 (1), 35–44 (1971). doi: 10.1093/oxfordjournals.jbchem.a129624
  4. Shimomura O., Johnson F. H., and Kohama Y. Reactions involved in bioluminescence systems of limpet (Latia neritoides) and luminous bacteria. Proc. Natl. Acad. Sci. USA., 69 (8), 2086–2089 (1972). doi: 10.1073/pnas.69.8.2086
  5. McCapra F. and Hysert D. W. Bacterial bioluminescenceidentification of fatty acid as product, its quantum yield and a suggested mechanism. Biochem. Biophys. Res. Commun., 52 (1), 298–304 (1973). doi: 10.1016/0006-291X(73)90987-X
  6. Sokolova I. V., Kalacheva G. S., and Tyulkova N. A. Analysis of the ratio of quantum yield and fatty acid formation of Photobacterium leiognathi bioluminescence. Vest. MGU. Khimiya, 41 (6), 118–120 (2000).
  7. Kaku T., Sugiura K., Entani, T., Osabe K., and Nagai T. Enhanced brightness of bacterial luciferase by bioluminescence resonance energy transfer. Sci. Rep., 11 (1), 14994 (2021). doi: 10.1038/s41598-02194551-4
  8. Kanosue Y., Kojima S., and Ohkata K. Influence of solvent viscosity on the rate of hydrolysis of dipeptides by carboxypeptidase Y. J. Phys. Org. Chem., 17 (5), 448–457 (2004). doi: 10.1002/poc.752
  9. Chen J., Kistemaker J. C., Robertus J., and Feringa B. L. Molecular stirrers in action. J. Am. Chem. Soc., 136 (42), 14924–14932 (2014). doi: 10.1021/ja507711h
  10. Adam W., Diedering M., and Trofimov A. A. V. Intriguing double‐inversion stereochemistry in the denitrogenation of 2, 3‐diazabicyclo[2.2.1]heptene‐type azoalkanes: a model mechanistic study in physical organic chemistry. J. Phys. Org. Chem., 17 (8), 643–655 (2004). doi: 10.1002/poc.834
  11. Adam W., Diedering, M., and Trofimov, A. V. Solvent effects in the photodenitrogenation of the azoalkane diazabicyclo[2.2.1]hept-2-ene: viscosity-and polaritycontrolled stereoselectivity in housane formation from the diazenyl diradical. Phys. Chem. Chem. Phys., 4, 1036–1039 (2002). doi: 10.1039/B110562K
  12. Лисица А. Е., Суковатый Л. А., Кратасюк В. А. и Немцева Е. В. Вязкие среды замедляют распад ключевого интермедиата биолюминесцентной реакции бактерий. Докл. РАН. Науки о жизни, 492 (1), 320–324 (2020). doi: 10.31857/S268673892002016X
  13. Lisitsa A. E., Sukovatyi L. A., Bartsev S. I., Deeva A. A., Kratasyuk V. A., and Nemtseva E. V. Mechanisms of viscous media effects on elementary steps of bacterial bioluminescent reaction. Int. J. Mol. Sci., 22 (16), 8827 (2021). doi: 10.3390/ijms22168827
  14. Lisitsa A. E., Sukovatyi L. A., Deeva A. A., Gulnov D. V., Esimbekova E. N., Kratasyuk V. A., and Nemtseva E. V. The Role of Cosolvent–Water Interactions in Effects of the Media on Functionality of Enzymes: A Case Study of Photobacterium leiognathi Luciferase. Life, 13 (6), 1384 (2023). doi: 10.3390/life13061384
  15. Waterhouse A., Bertoni M., Bienert S., Studer G., Tauriello G., Gumienny R., and Schwede T. SWISSMODEL: homology modelling of protein structures and complexes. Nucl. Acids Res., 46 (1) 296–303 (2018). doi: 10.1093/nar/gky427
  16. Campbell Z. T., Baldwin T. O., and Miyashita O. Analysis of the bacterial luciferase mobile loop by replicaexchange molecular dynamics. Biophys. J., 99, 4012 (2010). doi: 10.1016/j.bpj.2010.11.001
  17. Van Der Spoel D., Lindahl E., Hess B., Groenhof G., Mark A. E., and Berendsen H. J. GROMACS: fast, flexible, and free. J. Comput. Chem., 26 (16), 1701 (2005). doi: 10.1002/jcc.20291
  18. Kim S., Lee J., Jo S., Brooks C. L. III, Lee H. S., and Im W. CHARMM‐GUI ligand reader and modeler for CHARMM force field generation of small molecules. J. Comput. Chem, 38 (21), 1879–1886, (2017). doi: 10.1002/jcc.24829
  19. Michaud‐Agrawal N., Denning E. J., Woolf T. B., and Beckstein O. MDAnalysis: a toolkit for the analysis of molecular dynamics simulations. J. Comput. Chem, 32 (10), 2319–2327 (2011). doi: 10.1002/jcc.21787
  20. Gowers R. J., Linke M., Barnoud J., Reddy T. J. E., Melo M. N., Seyler S. L., Dotson D. L., Domanski J., Buchoux S., Kenney I. M., and Beckstein O. MDAnalysis, Proc. 15th Python Sci. Conf., 98, 105 (2016).
  21. Суковатый Л. А., Лисица А. Е., Кратасюк В. А. и Немцева Е. В. Влияние осмолитов на биолюминесцентную реакцию бактерий: структурно-динамические аспекты. Биофизика, 65 (6), 1135–1141 (2020). doi: 10.31857/S0006302920060137
  22. Deeva A. A., Lisitsa A. E., Sukovatyi L. A., MelnikT. N., Kratasyuk V. A., and Nemtseva E. V. Structure-function relationships in temperature effects on bacterial luciferases: Nothing is perfect. Int. J. Mol. Sci., 23 (15), 8119 (2022). doi: 10.3390/ijms23158119
  23. Deeva A. A., Temlyakova E. A., Sorokin A. A., Nemtseva E. V., and Kratasyuk V. A. Structural distinctions of fast and slow bacterial luciferases revealed by phylogenetic analysis. Bioinformatics, 32 (20), 3053–3057 (2016). doi: 10.1093/bioinformatics/btw386
  24. Суковатый Л. А., Молекулярно-динамический анализ влияния осмолитов на структуру бактериальных люцифераз, Дис. … канд. ф.-м. н. (Сибирский федеральный университет, 2023).
  25. Фонин А. В., Уверский В. Н., Кузнецова И. М. и Туроверов К. К. Фолдинг и стабильность белка в присутствии осмолитов. Биофизика, 61 (2), 222–230 (2016).
  26. Hastings J. W. and Gibson Q. H. Intermediates in the bioluminescent oxidation of reduced flavin mononucleotide. J. Biol. Chem., 238 (7), 2537–2554 (1963). doi: 10.1016/S0021-9258(19)68004-X
  27. Hastings J. W., Gibson Q. H., and Greenwood C. Evidence for high energy storage intermediates in bioluminescence. J. Photochem. Photobiol., 4 (6), 1227–1241 (1965). doi: 10.1111/j.1751-1097.1965.tb09309.x
  28. Lee J. Bacterial bioluminescence. Quantum yields and stoichiometry of the reactants reduced flavin mononucleotide, dodecanal, and oxygen, and of a product hydrogen peroxide. Biochemistry, 11 (18), 3350–3359 (1972). doi: 10.1021/bi00768a007
  29. Nakamura A., Okumura J. I. and Muramatsu T. Quantitative analysis of luciferase activity of viral and hybrid promoters in bovine preimplantation embryos. Mol. Reprod. Dev., 49 (4), 368–373 (1998). doi: 10.1002/(SICI)1098-2795(199804)49:4<368::AIDMRD3>3.0.CO;2-L
  30. Hastings J. W., Balny C., Peuch C. L. and Douzou P. Spectral properties of an oxygenated luciferase—flavin intermediate isolated by low-temperature chromatography. Proc. Natl. Acad. Sci. USA, 70 (12), 3468–3472 (1973). doi: 10.1073/pnas.70.12.3468
  31. Tang Y. Q., Luo Y., Liu Y. J. Theoretical study on role of aliphatic aldehyde in bacterial bioluminescence. J. Photochem. Photobiol. A, 419, 113446 (2021). doi: 10.1016/j.jphotochem.2021.113446
  32. Tinikul R., Lawan N., Akeratchatapan N., Pimviriyakul P., Chinantuya W., Suadee C., Sucharitakul J., Chenprakhon P., Ballou D. P., and Entsch B. Protonation status and control mechanism of flavin–oxygen intermediates in the reaction of bacterial luciferase. FEBS J., 288 (10), 3246–3260 (2021). doi: 10.1111/febs.15653
  33. Luo Y. and Liu Y. J. Revisiting the origin of bacterial bioluminescence: QM/MM study on oxygenation reaction of reduced flavin in protein. ChemPhysChem, 20 (3), 405-409 (2019). doi: 10.1002/cphc.201800970
  34. Lovell S. C., Word J. M., Richardson J. S., and Richardson D. C. The penultimate rotamer library. Prot. Struct. Funct. Bioinf., 40 (3), 389–408 (2000). doi: 10.1002/1097-0134(20000815)40:3<389::AIDPROT50>3.0.CO;2-2

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