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The influence of base pair tautomerism on single point mutations in aqueous DNA

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Gheorghiu, A., Coveney, P. V., Arabi, A. A.·2020·Interface Focus
DOI 10.1098/rsfs.2019.0120PMC PMC7653342
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Abstract

The relationship between base pair hydrogen bond proton transfer and the rate of spontaneous single point mutations at ambient temperatures and pressures in aqueous DNA is investigated. By using an ensemble-based multiscale computational modelling method, statistically robust rates of proton transfer for the A:T and G:C base pairs within a solvated DNA dodecamer are calculated. Several different proton transfer pathways are observed within the same base pair. It is shown that, in G:C, the double proton transfer tautomer is preferred, while the single proton transfer process is favoured in A:T. The reported range of rate coefficients for double proton transfer is consistent with recent experimental data. Notwithstanding the approximately 1000 times more common presence of single proton transfer products from A:T, observationally there is bias towards G:C to A:T mutations in a wide range of living organisms. We infer that the double proton transfer reactions between G:C base pairs have a negligible contribution towards this bias for the following reasons: (i) the maximum half-life of the G*:C* tautomer is in the range of picoseconds, which is significantly smaller than the milliseconds it takes for DNA to unwind during replication, (ii) statistically, the majority of G*:C* tautomers revert back to their canonical forms through a barrierless process, and (iii) the thermodynamic instability of the tautomers with respect to the canonical base pairs. Through similar reasoning, we also deduce that proton transfer in the A:T base pair does not contribute to single point mutations in DNA.

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  • The tautomeric state A*-T* is extremely unstable, with a fleetingly short lifetime, and therefore not as likely to play a role in mutagenesis.

    “Our decision to study G-C rather than A-T is because the tautomeric state, A*-T*, is extremely unstable, with a fleetingly short lifetime, and therefore not as likely to play a role in mutagenesis 4,5,7,13 .”

    From An open quantum systems approach to proton tunnelling in DNA (2022) · cites this paper as [7]

    The Results and discussion describe A*:T* as highly unstable, and the Conclusion estimates its equilibrium abundance to be negligible, supporting a limited role in mutagenesis. But the paper does not establish a fleetingly short lifetime for A*:T*: the approximately 6 fs half-life reported in Results and discussion belongs to the distinct A+:T− zwitterion, while rate coefficients for A*:T* were not determined. Page numbers are unavailable in our copy. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • In the standard Watson-Crick configuration, the formation of the single proton transfer is either unstable or energetically unfavourable.

    “The argument is that in the standard Watson-Crick configuration, the formation of the single proton transfer is either unstable or energetically unfavourable 5,7,11,12 .”

    From An open quantum systems approach to proton tunnelling in DNA (2022) · cites this paper as [7]

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Authors
Gheorghiu, A., Coveney, P. V., & Arabi, A. A.
Affiliations
  • University College London (GB)
  • United Arab Emirates University (AE)
Corresponding author
  • Coveney, P. V.
  • Arabi, A. A.
ORCID
Venue
Interface Focus
Publisher
The Royal Society
Published
2020-10-16
Volume
10
Issue
6
Pages
20190120-20190120
ISSN
  • 2042-8898 (ISSN-L)
  • 2042-8901
DOI
10.1098/rsfs.2019.0120
PMC
PMC7653342
OpenAlex
W3104801205
Cited by
52
References
8
Citations by year
2026: 7 · 2025: 8 · 2024: 5 · 2023: 17 · 2022: 9 · 2021: 4 · 2020: 2
FWCI
2.60
Type
journal article
Language
en
Open access
Licence
Locations
  • Interface Focus (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • UCL Provost
  • Engineering and Physical Sciences Research Council (EP/R029598/1)
  • Zayed University
  • Medical Research Council (MR/L016311/1)
  • Horizon 2020 Framework Programme (675451, 800925, 823712)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Physical Sciences › Chemistry › Organic Chemistry › Chemical Reaction Mechanisms
Keywords
point mutations, spontaneous mutation, GC base pairs, AT base pairs, double proton transfer, DNA dodecamer, mutational bias, DNA replication

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