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Action spectroscopy of isomer-selected luciferin anions

  • Regular Article - Molecular Physics and Chemical Physics
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Abstract

Luciferin molecules are common luminophores found throughout the biological kingdoms. Here, electrospray ionization and tandem ion mobility spectrometry coupled with laser spectroscopy are used to demonstrate that D-luciferin and oxyluciferin deprotonated anions can be produced in two isomeric forms, which can be separated by virtue of their different collision cross sections with a buffer gas. The two isomers possess distinguishable but partially overlapping photodepletion action spectra over the visible range, implying distinct intrinsic absorption profiles. The site of deprotonation and tautomeric forms of the electrosprayed isomers are assigned through comparisons between experimental and calculated collision cross sections and electronic excitation energies. The study clearly shows that electrospray ionization of biochromophore molecules can generate multiple isomeric forms with distinct electronic spectra.

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Data Availability Statement

This manuscript has data included as electronic supplementary material.

References

  1. V.R. Viviani, Cell. Mol. Life Sci. 59, 1833 (2002)

    Article  Google Scholar 

  2. T. Wilson, J.W. Hastings, Bioluminescence: Living Lights, Lights for Living (Harvard University Press, Harvard, 2013)

    Book  Google Scholar 

  3. G.C. Van de Bittner, E.A. Dubikovskaya, C.R. Bertozzi, C.J. Chang, Proc. Nat. Acad. Sci. 107, 21316 (2010)

    Article  ADS  Google Scholar 

  4. A. Schena, R. Griss, K. Johnsson, Nat. Commun. 6, 7830 (2015)

    Article  ADS  Google Scholar 

  5. J. Li, L. Chen, L. Dua, M. Li, Chem. Soc. Rev. 42, 662 (2013)

    Article  Google Scholar 

  6. H. Fraga, Photochem. Photobio. Sci. 7, 146 (2008)

    Article  Google Scholar 

  7. A. Roda, M. Guardigli, E. Michelini, M. Mirasoli, Trends. Anal. Chem. 28, 307 (2009)

    Google Scholar 

  8. D. Scott, E. Dikici, M. Ensor, S. Daunert, Ann. Rev. Anal. Chem. 4, 297 (2011)

    Article  Google Scholar 

  9. K. Gomi, N. Kajiyama, J. Biol. Chem. 276, 36508 (2001)

    Article  Google Scholar 

  10. H.H. Seliger, W.D. McElroy, Proc. Nat. Acad. Sci. 52, 75 (1964)

    Article  ADS  Google Scholar 

  11. A.B. Lall, H.H. Seliger, W.H. Biggley, J.E. Lloyd, Science 210, 560 (1980)

    Article  ADS  Google Scholar 

  12. T. Nakatsu, S. Ichiyama, J. Hiratake, A. Saldanha, N. Kobashi, K. Sakata, H. Kato, Nature 440, 372 (2006)

    Article  ADS  Google Scholar 

  13. S. Hosseinkhani, Cell. Mol. Life Sci. 68, 1167 (2011)

    Article  Google Scholar 

  14. P.H. Liua, P.L. Urban, Anal. Biochem. 593, 54 (2017)

    Google Scholar 

  15. V.R. Viviani, F.G.C. Arnoldi, A.J.S. Neto, T.L. Oehlmeyer, E.J.H. Becharae, Y. Ohmiya, Photochem. Photobiol. Sci. 7, 159 (2008)

    Article  Google Scholar 

  16. Y. Ando, K. Niwa, N. Yamada, T. Enomoto, T. Irie, H. Kubota, Y. Ohmiya, H. Akiyama, Nat. Photon. 2, 44 (2008)

    Article  ADS  Google Scholar 

  17. P. Gosset, G. Taupier, O. Crégut, J. Brazard, Y. Mély, K.D. Dorkenoo, J. Léonard, P. Didier, J. Phys. Chem. Lett. 11, 3653 (2020)

    Article  Google Scholar 

  18. K. Støchkel, B.F. Milne, S.B. Nielsen, J. Phys. Chem. A 115, 2155 (2011)

    Article  Google Scholar 

  19. K. Støchkel, C.N. Hansen, J. Houmøller, L.M. Nielsen, K. Anggara, M. Linares, P. Norman, F. Nogueira, O.V. Maltsev, L. Hintermann, S.B. Nielsen, P. Naumov, B.F. Milne, J. Am. Chem. Soc. 135, 6485 (2013)

    Article  Google Scholar 

  20. J.L. Woodhouse, M. Assmann, M.A. Parkes, H. Grounds, S.J. Pacman, J.C. Anderson, G.A. Worth, H.H. Fielding, Phys. Chem. Chem. Phys. 19, 22711 (2017)

    Article  Google Scholar 

  21. A.M. Patel, A. Henley, M.A. Parkes, M. Assmann, G.A. Worth, J.C. Anderson, H.H. Fielding, Phys. Chem. Chem. Phys. 22, 19022 (2020)

    Article  Google Scholar 

  22. B.D. Adamson, N.J.A. Coughlan, R.E. Continetti, E.J. Bieske, Phys. Chem. Chem. Phys. 15, 9540 (2013)

    Article  Google Scholar 

  23. B.D. Adamson, N.J.A. Coughlan, P.B. Markworth, R.E. Continetti, E.J. Bieske, Rev. Sci. Inst. 85, 123109 (2014)

    Article  ADS  Google Scholar 

  24. J.N. Bull, E. Carrascosa, N. Mallo, M.S. Scholz, G. da Silva, J.E. Beves, E.J. Bieske, J. Phys. Chem. Lett. 9, 665 (2018)

    Article  Google Scholar 

  25. J.N. Bull, G. da Silva, M.S. Scholz, E. Carrascosa, E.J. Bieske, J. Phys. Chem. A 123, 4419 (2019)

    Article  Google Scholar 

  26. J.N. Bull, J.T. Buntine, M.S. Scholz, E. Carrascosa, L. Giacomozzi, M.H. Stockett, E.J. Bieske, Faraday Discuss. 217, 34 (2019)

    Article  ADS  Google Scholar 

  27. G.A. Eiceman, Z. Karpas, H.H. Hill, Ion Mobility Spectrometry, 3rd edn. (CRC Press, Boca Raton, 2013)

    Book  Google Scholar 

  28. M.J. Frisch, G.W. Trucks, H.B. Schlegel, G.E. Scuseria, M.A. Robb, J.R. Cheeseman, G. Scalmani, V. Barone, B. Mennucci, G.A. Petersson, H. Nakatsuji, M. Caricato, X. Li, H.P. Hratchian, A.F. Izmaylov, J. Bloino, G. Zheng, J.L. Sonnenberg, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao, H. Nakai, T. Vreven, J.A. Montgomery, Jr., J.E. Peralta, F. Ogliaro, M. Bearpark, J.J. Heyd, E. Brothers, K.N. Kudin, V.N. Staroverov, R. Kobayashi, J. Normand, K. Raghavachari, A. Rendell, J.C. Burant, S.S. Iyengar, J. Tomasi, M. Cossi, N. Rega, J.M. Millam, M. Klene, J.E. Knox, J.B. Cross, V. Bakken, C. Adamo, J. Jaramillo, R. Gomperts, R.E. Stratmann, O. Yazyev, A.J. Austin, R. Cammi, C. Pomelli, J.W. Ochterski, R.L. Martin, K. Morokuma, V.G. Zakrzewski, G.A. Voth, P. Salvador, J.J. Dannenberg, S. Dapprich, A.D. Daniels, Ö. Farkas, J.B. Foresman, J.V. Ortiz, J. Cioslowski, D.J. Fox. Gaussian 16 Revision A.03. Gaussian Inc. Wallingford CT 2016

  29. F. Neese, WIRES Comp. Mol. Sci. 2, 73 (2012)

    Article  Google Scholar 

  30. M. Kállay, Z. Rolik, J. Csontos, P. Nagy, G. Samu, D. Mester, I. Ladjánszki, L. Szegedy, B. Ladóczki, K. Petrov, M. Farkas, B. Hégely. MRCC, A Quantum Chemical Program Suite. www.mrcc.hu

  31. J.D. Chai, M. Head-Gordon, Phys. Chem. Chem. Phys. 10, 6615 (2008)

    Article  Google Scholar 

  32. T.H. Dunning Jr., J. Chem. Phys. 90, 1007 (1989)

    Article  ADS  Google Scholar 

  33. C. Riplinger, B. Sandhoefer, A. Hansen, F. Neese, J. Chem. Phys. 139, 134101 (2013)

    Article  ADS  Google Scholar 

  34. C. Hättig, F. Weigend, J. Chem. Phys. 113, 5154 (2000)

    Article  ADS  Google Scholar 

  35. A.K. Dutta, M. Saitow, B. Demoulin, F. Neese, R. Izsák, J. Chem. Phys. 150, 164123 (2019)

    Article  ADS  Google Scholar 

  36. I. Campuzano, M.F. Bush, C.V. Robinson, C. Beaumont, K. Richardson, H. Kim, H.I. Kim, Anal. Chem. 84(2), 1026 (2012)

    Article  Google Scholar 

  37. M.F. Mesleh, J.M. Hunter, A.A. Shvartsburg, G.C. Schatz, M.F. Jarrold, J. Phys. Chem. 100(40), 16082 (1996)

    Article  Google Scholar 

  38. B.H. Besler, K.M. Merz Jr., P.A. Kollman, J. Comp. Chem. 11, 431 (1990)

    Article  Google Scholar 

  39. J.N. Bull, M.S. Scholz, E. Carrascosa, G. da Silva, E.J. Bieske, Phys. Rev. Lett. 120, 223002 (2018)

    Article  ADS  Google Scholar 

  40. E. Carrascosa, J.N. Bull, M.S. Scholz, N.J.A. Coughlan, S. Olsen, U. Wille, E.J. Bieske, J. Phys. Chem. Lett. 9, 2647 (2018)

    Article  Google Scholar 

  41. J.N. Bull, E. Carrascosa, L. Giacomozzi, E.J. Bieske, M.H. Stockett, Phys. Chem. Chem. Phys. 20, 19672 (2018)

    Article  Google Scholar 

  42. M. Almasian, J. Grzetic, J. van Maurik, J.D. Steill, G. Berden, S. Ingemann, W.J. Buma, J. Oomens, J. Phys. Chem. Lett. 3, 2259 (2012)

    Article  Google Scholar 

  43. J.N. Bull, C.W. West, C.S. Anstöter, G. da Silva, E.J. Bieske, J.R.R. Verlet, Phys. Chem. Chem. Phys. 21, 10567 (2019)

    Article  Google Scholar 

  44. N.J.A. Coughlan, B.D. Adamson, L. Gamon, K. Catani, E.J. Bieske, Phys. Chem. Chem. Phys. 17, 22623 (2015)

    Article  Google Scholar 

  45. H. Xia, A.B. Attygalle, Anal. Chem. 88, 6035 (2016)

    Article  Google Scholar 

  46. A.B. Attygalle, H. Xia, J. Pavlov, J. Am. Soc. Mass Spectrom. 28, 1575 (2017)

    Article  ADS  Google Scholar 

  47. H. Xia, A.B. Attygalle, J. Am. Soc. Mass Spectrom. 28, 2580 (2017)

    Article  ADS  Google Scholar 

  48. M.W. Jensen, K. Støchkel, C. Kjær, J.L. Knudsen, O.V. Maltsev, L. Hintermann, P. Naumov, B.F. Milne, S.B. Nielsen, Int. J. Mass Spectrom. 365–366, 3 (2014)

    Article  Google Scholar 

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Acknowledgements

This research was supported under the Australian Research Council’s Discovery Project funding scheme (DP150101427 and DP160100474). Electronic structure calculations were carried out on the High Performance Computing Cluster supported by the Research and Specialist Computing Support service at the University of East Anglia. CK thanks Augustinus Fonden, Niels Bohr Fondet and Oticon Fonden for travel support. EC acknowledges support by the Austrian Science Fund (FWF) through a Schrödinger Fellowship (Nr. J4013-N36).

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Action spectroscopy experiments were performed by CK, JNB and EC in the laboratory of EJB. Calculations were performed by CK and JNB. The manuscript was drafted by JNB with contributions from all authors.

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Correspondence to Evan J. Bieske.

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Kjær, C., Bull, J.N., Carrascosa, E. et al. Action spectroscopy of isomer-selected luciferin anions. Eur. Phys. J. D 75, 72 (2021). https://doi.org/10.1140/epjd/s10053-021-00076-w

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