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

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

Research output: Contribution to journalArticle

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.
LanguageEnglish
Number of pages10
JournalPhysical Chemistry Chemical Physics
StateAccepted/In press - 3 Apr 2017

Fingerprint

Optical Kerr effect
dynamic structural analysis
Structural dynamics
Kerr effects
Melting
deoxyribonucleic acid
melting
Spectroscopy
DNA
spectroscopy
Single-Stranded DNA
helices
vibration mode
Molecular recognition
Solvation
Hydration
Energy transfer
spine
Melting point
Infrared spectroscopy

Keywords

  • solvation dynamics
  • DNA
  • deoxyribonucleic acid
  • structural dynamics
  • ultrafast two-dimensional infrared spectroscopy
  • 2D-IR
  • optical Kerr-effect spectroscopy
  • OKE

Cite this

Hithell, G., González-Jiménez, M., Greetham, G. M., Donaldson, P. M., Towrie, M., Parker, A. W., ... Hunt, N. (Accepted/In press). Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA. Physical Chemistry Chemical Physics.
Hithell, Gordon ; González-Jiménez, Mario ; Greetham, Gregory M. ; Donaldson, Paul M. ; Towrie, Michael ; Parker, Anthony W. ; Burley, Glenn A. ; Wynne, Klaas ; Hunt, Neil. / Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA. In: Physical Chemistry Chemical Physics. 2017
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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.",
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author = "Gordon Hithell and Mario Gonz{\'a}lez-Jim{\'e}nez and Greetham, {Gregory M.} and Donaldson, {Paul M.} and Michael Towrie and Parker, {Anthony W.} and Burley, {Glenn A.} and Klaas Wynne and Neil Hunt",
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Hithell, G, González-Jiménez, M, Greetham, GM, Donaldson, PM, Towrie, M, Parker, AW, Burley, GA, Wynne, K & Hunt, N 2017, 'Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA' Physical Chemistry Chemical Physics.

Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA. / Hithell, Gordon; González-Jiménez, Mario; Greetham, Gregory M.; Donaldson, Paul M.; Towrie, Michael; Parker, Anthony W.; Burley, Glenn A.; Wynne, Klaas; Hunt, Neil.

In: Physical Chemistry Chemical Physics, 03.04.2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Ultrafast 2D-IR and optical Kerr effect spectroscopy reveal the impact of duplex melting on the structural dynamics of DNA

AU - Hithell,Gordon

AU - González-Jiménez,Mario

AU - Greetham,Gregory M.

AU - Donaldson,Paul M.

AU - Towrie,Michael

AU - Parker,Anthony W.

AU - Burley,Glenn A.

AU - Wynne,Klaas

AU - Hunt,Neil

PY - 2017/4/3

Y1 - 2017/4/3

N2 - 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.

AB - 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.

KW - solvation dynamics

KW - DNA

KW - deoxyribonucleic acid

KW - structural dynamics

KW - ultrafast two-dimensional infrared spectroscopy

KW - 2D-IR

KW - optical Kerr-effect spectroscopy

KW - OKE

UR - http://www.rsc.org/journals-books-databases/about-journals/PCCP/

M3 - Article

JO - Physical Chemistry Chemical Physics

T2 - Physical Chemistry Chemical Physics

JF - Physical Chemistry Chemical Physics

SN - 1463-9076

ER -