On the influence of water on the electronic structure of firefly oxyluciferin anions from absorption spectroscopy of bare and monohydrated ions in vacuo

Kristian Støchkel, Christian Nygaard Hansen, Jørgen Houmøller, Lisbeth Munksgaard Nielsen, Kelvin Anggara, Mathieu Linares, Patrick Norman, Fernando Nogueira, Oleg V. Maltsev, Lukas Hintermann, Steen Brøndsted Nielsen, Pance Naumov, Bruce F. Milne

Research output: Contribution to journalArticle

Abstract

A complete understanding of the physics underlying the varied colors of firefly bioluminescence remains elusive because it is difficult to disentangle different enzyme-lumophore interactions. Experiments on isolated ions are useful to establish a proper reference when there are no microenvironmental perturbations. Here, we use action spectroscopy to compare the absorption by the firefly oxyluciferin lumophore isolated in vacuo and complexed with a single water molecule. While the process relevant to bioluminescence within the luciferase cavity is light emission, the absorption data presented here provide a unique insight into how the electronic states of oxyluciferin are altered by microenvironmental perturbations. For the bare ion we observe broad absorption with a maximum at 548 ± 10 nm, and addition of a water molecule is found to blue-shift the absorption by approximately 50 nm (0.23 eV). Test calculations at various levels of theory uniformly predict a blue-shift in absorption caused by a single water molecule, but are only qualitatively in agreement with experiment highlighting limitations in what can be expected from methods commonly used in studies on oxyluciferin. Combined molecular dynamics simulations and time-dependent density functional theory calculations closely reproduce the broad experimental peaks and also indicate that the preferred binding site for the water molecule is the phenolate oxygen of the anion. Predicting the effects of microenvironmental interactions on the electronic structure of the oxyluciferin anion with high accuracy is a nontrivial task for theory, and our experimental results therefore serve as important benchmarks for future calculations.

Original languageEnglish (US)
Pages (from-to)6485-6493
Number of pages9
JournalJournal of the American Chemical Society
Volume135
Issue number17
DOIs
StatePublished - May 1 2013

Fingerprint

Fireflies
Absorption spectroscopy
Electronic structure
Anions
Spectrum Analysis
Negative ions
Ions
Bioluminescence
Molecules
Water
Light emission
Electronic states
Binding sites
Benchmarking
Luciferases
Density functional theory
Physics
Molecular dynamics
Molecular Dynamics Simulation
Enzymes

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

On the influence of water on the electronic structure of firefly oxyluciferin anions from absorption spectroscopy of bare and monohydrated ions in vacuo. / Støchkel, Kristian; Hansen, Christian Nygaard; Houmøller, Jørgen; Nielsen, Lisbeth Munksgaard; Anggara, Kelvin; Linares, Mathieu; Norman, Patrick; Nogueira, Fernando; Maltsev, Oleg V.; Hintermann, Lukas; Nielsen, Steen Brøndsted; Naumov, Pance; Milne, Bruce F.

In: Journal of the American Chemical Society, Vol. 135, No. 17, 01.05.2013, p. 6485-6493.

Research output: Contribution to journalArticle

Støchkel, K, Hansen, CN, Houmøller, J, Nielsen, LM, Anggara, K, Linares, M, Norman, P, Nogueira, F, Maltsev, OV, Hintermann, L, Nielsen, SB, Naumov, P & Milne, BF 2013, 'On the influence of water on the electronic structure of firefly oxyluciferin anions from absorption spectroscopy of bare and monohydrated ions in vacuo', Journal of the American Chemical Society, vol. 135, no. 17, pp. 6485-6493. https://doi.org/10.1021/ja311400t
Støchkel, Kristian ; Hansen, Christian Nygaard ; Houmøller, Jørgen ; Nielsen, Lisbeth Munksgaard ; Anggara, Kelvin ; Linares, Mathieu ; Norman, Patrick ; Nogueira, Fernando ; Maltsev, Oleg V. ; Hintermann, Lukas ; Nielsen, Steen Brøndsted ; Naumov, Pance ; Milne, Bruce F. / On the influence of water on the electronic structure of firefly oxyluciferin anions from absorption spectroscopy of bare and monohydrated ions in vacuo. In: Journal of the American Chemical Society. 2013 ; Vol. 135, No. 17. pp. 6485-6493.
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AU - Nielsen, Lisbeth Munksgaard

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AU - Linares, Mathieu

AU - Norman, Patrick

AU - Nogueira, Fernando

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