Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA.

Gordon Hithell,Gregory M Greetham,Klaas Wynne,Anthony W Parker,Michael Towrie,Glenn A Burley,Paul M Donaldson,Mario González-Jiménez,Neil T Hunt

doi:10.1039/c7cp00054e

Abstract

Changes in the structural and solvation dynamics of a 15mer AT DNA duplex upon melting of the double-helix are observed by a combination of ultrafast two-dimensional infrared (2D-IR) and optical Kerr-effect (OKE) spectroscopies. 2D-IR spectroscopy of the vibrational modes of the DNA bases reveal signature off-diagonal peaks arising from coupling and energy transfer across Watson-Crick paired bases that are unique to double-stranded DNA (ds-DNA). Spectral diffusion of specific base vibrational modes report on the structural dynamics of the duplex and the minor groove, which is predicted to contain a spine of hydration. Changes in these dynamics upon melting are assigned to increases in the degree of mobile solvent access to the bases in single-stranded DNA (ss-DNA) relative to the duplex. OKE spectra exhibit peaks that are assigned to specific long-range phonon modes of ds- and ss-DNA. Temperature-related changes in these features correlate well with those obtained from the 2D-IR spectra although the melting temperature of the ds-DNA phonon band is slightly higher than that for the Watson-Crick modes, suggesting that a degree of long-range duplex structure survives the loss of Watson-Crick hydrogen bonding. These results demonstrate that the melting of ds-DNA disrupts helix-specific structural dynamics encompassing length scales ranging from mode delocalisation in the Watson-Crick base pairs to long-range phonon modes that extend over multiple base pairs and which may play a role in molecular recognition of DNA.

Highlights

Deoxyribonucleic acid (DNA)-recognition and the conformational changes that occur upon binding remains to be established.[6]
Changes in the structural and solvation dynamics of a 15mer AT DNA duplex upon melting of the double-helix are observed by a combination of ultrafast two-dimensional infrared (2D-IR) and optical Kerr-effect (OKE) spectroscopies. 2D-IR spectroscopy of the vibrational modes of the DNA bases reveal signature off-diagonal peaks arising from coupling and energy transfer across Watson–Crick paired bases that are unique to double-stranded DNA
These results demonstrate that the melting of double-stranded DNA (ds-DNA) disrupts helix-specific structural dynamics encompassing length scales ranging from mode delocalisation in the Watson–Crick base pairs to long-range phonon modes that extend over multiple base pairs and which may play a role in molecular recognition of DNA

Summary

Introduction

DNA-recognition and the conformational changes that occur upon binding remains to be established.[6] This shows that other factors need to be considered and we suggest that these include the action of molecular dynamics.[7] DNA is a highly dynamic molecule where considerable unwinding of the duplex plays essential roles in the transcription and replication processes. Underpinning these functions is the effect of the aqueous physiological environment. The Watson– Crick hydrogen-bonding interaction has been shown to induce vibrational coupling and delocalisation of vibrational modes across the base pair,[8,9,10,11,12] while base–base-interactions along the strand contribute to the overall thermal stability of the double helix.[13,14] Recently, we have found evidence that base vibrational modes couple to those of the backbone in the double helix structure, while energy relaxation follows a cascade from

Methods

Results

Discussion

Conclusion