Unveiled electric profiles within hydrogen bonds suggest DNA base pairs with similar bond strengths

Abstract

Electrical forces are the background of all the interactions occurring in biochemical systems. From here and by using a combination of ab-initio and ad-hoc models, we introduce the first description of electric field profiles with intrabond resolution to support a characterization of single bond forces attending to its electrical origin. This fundamental issue has eluded a physical description so far. Our method is applied to describe hydrogen bonds (HB) in DNA base pairs. Numerical results reveal that base pairs in DNA could be equivalent considering HB strength contributions, which challenges previous interpretations of thermodynamic properties of DNA based on the assumption that Adenine/Thymine pairs are weaker than Guanine/Cytosine pairs due to the sole difference in the number of HB. Thus, our methodology provides solid foundations to support the development of extended models intended to go deeper into the molecular mechanisms of DNA functioning.

Fig 1. Schematic representation for HB connecting base pairs in DNA.

a, b) A/T pair models. c, d) C/G pair models. On the left panels the atomistic structural representations are included. HB are labelled as HB₁, HB₂, HB₃, HB₄ and HB₅ throughout this work. On the right panels we include a diagram of the reduced elastic configuration we have used. A, T, G, and C basis are considered as rigid 2D boxes with identical mechanical responses. Then, the differences regarding molecular strengths will be originated on the 1D springs modelling HB.

Fig 2. On the electrical nature of a HB.

a, Standard dipole model for a HB where two opposite charges represent the interaction. Here and then, H, N and O indicate the position of hydrogen, nitrogen and oxygen atoms respectively. E is the vector representing the electric field in the main axis, Φ the deviation angle, di is the inflection point and d is the axis containing the two atoms involved in the HB. b, Our proposed electrostatic model for a HB interaction, two positive charges surrounded by an electron cloud, details in the main text. c, Heaviside representation for Φ = Φ (d), the behaviour expected for the model included in b) in the absence of electron cloud. d, Representation of the model included in b) approached as a limiting Heaviside function, see eq. S2 in the S3 File for the definition of finite t = ta values.

Fig 3. Electrical characterization of inter pairs HB in a model A/T base comparing with the HB stabilizing a water dimer sample.

In a) and b), we represent the variations of the electric field modulus (|E|) along the two-atom axis. The asymptotic behaviour coincides with atomic positions, positive charge centres with the coordinates origin in the atom, O or N, bridging the hydrogen atom. The existence of finite non-zero minimum values (|E|_threshold ~ 10 V nm-1) is essential for understanding the electrical inertia as well as the mechanical response originated in DNA. c) and d), show the characteristic evolution of the angle between E relative to the two atom axis, Φ = Φ(d). The deviations of such curves from the ideal Heaviside function are an indication of the electric susceptibility of chemical bonds, more details are included in the main text. The descriptors included in the inserted table accounts for electromechanical information. The numerical values, compared with the HB the water dimer (t_a(wd)) are indicative of superior strengths in the HB pairing A/T than in the HB forming the water dimer. See S2 File for details on the calculation of the water dimer parameters.

Fig 4. Electrical characterization of inter pairs HB in a model G/C base comparing with the HB stabilizing a water dimer sample.

In line with the reasoning included in Fig 3, in a) and b), we represent the variations of the electric field modulus (|E|) along the two-atom axis. In c) and d), show the characteristic evolution of the angle between E the two atom axis, Φ = Φ(d).