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DPT tautomerization of the long A∙A* Watson-Crick base pair formed by the amino and imino tautomers of adenine: combined QM and QTAIM investigation

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Abstract

Combining quantum-mechanical (QM) calculations with quantum theory of atoms in molecules (QTAIM) and using the methodology of sweeps of the energetic, electron-topological, geometric and polar parameters, which describe the course of the tautomerization along the intrinsic reaction coordinate (IRC), we showed for the first time that the biologically important A∙A* base pair (Cs symmetry) formed by the amino and imino tautomers of adenine (A) tautomerizes via asynchronous concerted double proton transfer (DPT) through a transition state (TS), which is the A+∙A− zwitterion with the separated charge, with Cs symmetry. The nine key points, which can be considered as electron-topological “fingerprints” of the asynchronous concerted A∙A*↔A*∙A tautomerization process via the DPT, were detected and completely investigated along the IRC of the A∙A*↔A*∙A tautomerization. Based on the sweeps of the H-bond energies, it was found that intermolecular antiparallel N6Н⋯N6 (7.01 kcal mol−1) and N1H⋯N1 (6.88 kcal mol−1) H-bonds are significantly cooperative and mutually reinforce each other. It was shown for the first time that the A∙A*↔A*∙A tautomerization is assisted by the third C2H⋯HC2 dihydrogen bond (DHB), which, in contrast to the two others N6H⋯N6 and N1H⋯N1 H-bonds, exists within the IRC range from −2.92 to 2.92 Å. The DHB cooperatively strengthens, reaching its maximum energy 0.42 kcal mol−1 at IRC = −0.52 Å and minimum energy 0.25 kcal mol−1 at IRC = −2.92 Å, and is accompanied by strengthening of the two other aforementioned classical H-bonds. We established that the C2H⋯HC2 DHB completely satisfies the electron-topological criteria for H-bonding, in particular Bader’s and all eight “two-molecule” Koch and Popelier’s criteria. The positive value of the Grunenberg’s compliance constant (5.203 Å/mdyn) at the TSA∙A*↔A*∙A proves that the C2H⋯HC2 DHB is a stabilizing interaction. NBO analysis predicts transfer of charge from σ(C2–H) bonding orbital to σ*(H–C2) anti-bonding orbital; at this point, the stabilization energy E(2) is equal to 0.19 kcal mol−1 at the TSA∙A*↔A*∙A.

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Acknowledgments

This work was partially supported by the Science and Technology Center in Ukraine (STCU) within the project № 5728 for years 2012–2014. O.O.B. was supported by a Grant of the President of Ukraine to support scientific research of young scientists for 2012 year from the State Fund for Fundamental Research of Ukraine (project № GP/F44/086) and by a Grant of the President of Ukraine for talented youth for year 2012 from the Ministry of Education and Science, Youth and Sports of Ukraine. The authors thank the Bogolyubov Institute for Theoretical Physics of the National Academy of Sciences of Ukraine for providing calculation resources and software. This work was performed using computational facilities of joint computer cluster of SSI “Institute for Single Crystals” of the National Academy of Sciences of Ukraine and Institute for Scintillation Materials of the National Academy of Sciences of Ukraine incorporated into Ukrainian National Grid.

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  1. Department of Molecular and Quantum Biophysics, Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, 150 Zabolotnoho Str, 03680, Kyiv, Ukraine

    Ol’ha O. Brovarets’, Roman O. Zhurakivsky & Dmytro M. Hovorun

  2. Research and Educational Center “State Key Laboratory of Molecular and Cell Biology”, 150 Zabolotnoho Str, 03680, Kyiv, Ukraine

    Ol’ha O. Brovarets’, Roman O. Zhurakivsky & Dmytro M. Hovorun

  3. Department of Molecular Biology, Biotechnology and Biophysics, Institute of High Technologies, Taras Shevchenko National University of Kyiv, 2 Hlushkova Ave, 03127, Kyiv, Ukraine

    Ol’ha O. Brovarets’ & Dmytro M. Hovorun

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  1. Ol’ha O. Brovarets’
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Brovarets’, O.O., Zhurakivsky, R.O. & Hovorun, D.M. DPT tautomerization of the long A∙A* Watson-Crick base pair formed by the amino and imino tautomers of adenine: combined QM and QTAIM investigation. J Mol Model 19, 4223–4237 (2013). https://doi.org/10.1007/s00894-013-1880-2

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