Low-frequency vibrational modes in G-quadruplexes reveal the mechanical properties of nucleic acids
Low-frequency vibrations play an essential role in biomolecular processes involving DNA such as gene expression, charge transfer, drug intercalation, and DNA-protein recognition. However, understanding of the vibrational basis of these mechanisms relies on theoretical models due to the lack of exper...
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| Abstract | Low-frequency vibrations play an essential role in biomolecular processes involving DNA such as gene expression, charge transfer, drug intercalation, and DNA-protein recognition. However, understanding of the vibrational basis of these mechanisms relies on theoretical models due to the lack of experimental evidence. Here we present the low-frequency vibrational spectra of G-quadruplexes (structures formed by four strands of DNA) and B-DNA characterized using femtosecond optical Kerr-effect spectroscopy. Contrary to expectation, we found that G-quadruplexes show several strongly underdamped delocalized phonon-like modes that have the potential to contribute to the biology of the DNA at the atomic level. In addition, G-quadruplexes present modes at a higher frequency than B-DNA demonstrating that changes in the stiffness of the molecule alter its gigahertz to terahertz vibrational profile. These results demonstrate that current theoretical models fail to predict basic properties of the vibrational modes of DNA. |
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| AbstractList | Low-frequency vibrations play an essential role in biomolecular processes involving DNA such as gene expression, charge transfer, drug intercalation, and DNA–protein recognition. However, understanding of the vibrational basis of these mechanisms relies on theoretical models due to the lack of experimental evidence. Here we present the low-frequency vibrational spectra of G-quadruplexes (structures formed by four strands of DNA) and B-DNA characterized using femtosecond optical Kerr-effect spectroscopy. Contrary to expectation, we found that G-quadruplexes show several strongly underdamped delocalized phonon-like modes that have the potential to contribute to the biology of the DNA at the atomic level. In addition, G-quadruplexes present modes at a higher frequency than B-DNA demonstrating that changes in the stiffness of the molecule alter its gigahertz to terahertz vibrational profile. These results demonstrate that current theoretical models fail to predict basic properties of the vibrational modes of DNA.
A number of recent studies have identified thermally excited low-frequency vibrational modes as a key deciding factor in the biological function of DNA. However, the nature of these vibrational modes has never been established. Here, vibrational spectroscopy with unrivalled signal-to-noise in the gigahertz to terahertz range is used to determine the low-frequency Raman spectra of nucleotides and oligomeric DNAs carefully chosen to form G-quadruplexes, structures formed by four strands of DNA common in the genome. These G-quadruplexes exhibit an unusual group of highly-underdamped delocalized vibrational modes—not reproduced by any of the theoretical models in use—which are expected to be the thermally excited. This provides a new perspective on the role of low-frequency vibrational modes in protein interactions and allostery. Low-frequency vibrations play an essential role in biomolecular processes involving DNA such as gene expression, charge transfer, drug intercalation, and DNA-protein recognition. However, understanding of the vibrational basis of these mechanisms relies on theoretical models due to the lack of experimental evidence. Here we present the low-frequency vibrational spectra of G-quadruplexes (structures formed by four strands of DNA) and B-DNA characterized using femtosecond optical Kerr-effect spectroscopy. Contrary to expectation, we found that G-quadruplexes show several strongly underdamped delocalized phonon-like modes that have the potential to contribute to the biology of the DNA at the atomic level. In addition, G-quadruplexes present modes at a higher frequency than B-DNA demonstrating that changes in the stiffness of the molecule alter its gigahertz to terahertz vibrational profile. These results demonstrate that current theoretical models fail to predict basic properties of the vibrational modes of DNA. |
| Author | Ramakrishnan, Gopakumar Wynne, Klaas González-Jiménez, Mario |
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| DOI | 10.1101/2020.03.16.993873 |
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| Keywords | Raman spectroscopy Dynamics Nucleic acids |
| Language | English |
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| Title | Low-frequency vibrational modes in G-quadruplexes reveal the mechanical properties of nucleic acids |
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