Temperature-induced DNA density transition in phage λ capsid revealed with contrast-matching SANS
Villanueva Valencia, José Ramón LU ; Tsimtsirakis, Efthymios LU ; Krueger, Susan and Evilevitch, Alex LU
(2023)
In Proceedings of the National Academy of Sciences of the United States of America
120(45).
- Abstract
Structural details of a genome packaged in a viral capsid are essential for understanding how the structural arrangement of a viral genome in a capsid controls its release dynamics during infection, which critically affects viral replication. We previously found a temperature-induced, solid-like to fluid-like mechanical transition of packaged λ-genome that leads to rapid DNA ejection. However, an understanding of the structural origin of this transition was lacking. Here, we use small-angle neutron scattering (SANS) to reveal the scattering form factor of dsDNA packaged in phage λ capsid by contrast matching the scattering signal from the viral capsid with deuterated buffer. We used small-angle X-ray scattering and cryoelectron... (More)
Structural details of a genome packaged in a viral capsid are essential for understanding how the structural arrangement of a viral genome in a capsid controls its release dynamics during infection, which critically affects viral replication. We previously found a temperature-induced, solid-like to fluid-like mechanical transition of packaged λ-genome that leads to rapid DNA ejection. However, an understanding of the structural origin of this transition was lacking. Here, we use small-angle neutron scattering (SANS) to reveal the scattering form factor of dsDNA packaged in phage λ capsid by contrast matching the scattering signal from the viral capsid with deuterated buffer. We used small-angle X-ray scattering and cryoelectron microscopy reconstructions to determine the initial structural input parameters for intracapsid DNA, which allows accurate modeling of our SANS data. As result, we show a temperature-dependent density transition of intracapsid DNA occurring between two coexisting phases-a hexagonally ordered high-density DNA phase in the capsid periphery and a low-density, less-ordered DNA phase in the core. As the temperature is increased from 20 °C to 40 °C, we found that the core-DNA phase undergoes a density and volume transition close to the physiological temperature of infection (~37 °C). The transition yields a lower energy state of DNA in the capsid core due to lower density and reduced packing defects. This increases DNA mobility, which is required to initiate rapid genome ejection from the virus capsid into a host cell, causing infection. These data reconcile our earlier findings of mechanical DNA transition in phage.
(Less)
- author
- Villanueva Valencia, José Ramón
LU
; Tsimtsirakis, Efthymios
LU
; Krueger, Susan
and Evilevitch, Alex
LU
- organization
- publishing date
- 2023-11-07
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- Bacteriophage lambda/genetics, Capsid/chemistry, Temperature, Cryoelectron Microscopy, DNA, Viral/chemistry, Capsid Proteins/genetics
- in
- Proceedings of the National Academy of Sciences of the United States of America
- volume
- 120
- issue
- 45
- article number
- e2220518120
- publisher
- National Academy of Sciences
- external identifiers
-
- scopus:85175676175
- pmid:37903276
- ISSN
- 1091-6490
- DOI
- 10.1073/pnas.2220518120
- language
- English
- LU publication?
- yes
- id
- 689c5c0b-4be1-4520-b96c-bb10c57dfdc2
- date added to LUP
- 2023-11-09 11:26:16
- date last changed
- 2024-04-21 19:33:03
@article{689c5c0b-4be1-4520-b96c-bb10c57dfdc2,
abstract = {{<p>Structural details of a genome packaged in a viral capsid are essential for understanding how the structural arrangement of a viral genome in a capsid controls its release dynamics during infection, which critically affects viral replication. We previously found a temperature-induced, solid-like to fluid-like mechanical transition of packaged λ-genome that leads to rapid DNA ejection. However, an understanding of the structural origin of this transition was lacking. Here, we use small-angle neutron scattering (SANS) to reveal the scattering form factor of dsDNA packaged in phage λ capsid by contrast matching the scattering signal from the viral capsid with deuterated buffer. We used small-angle X-ray scattering and cryoelectron microscopy reconstructions to determine the initial structural input parameters for intracapsid DNA, which allows accurate modeling of our SANS data. As result, we show a temperature-dependent density transition of intracapsid DNA occurring between two coexisting phases-a hexagonally ordered high-density DNA phase in the capsid periphery and a low-density, less-ordered DNA phase in the core. As the temperature is increased from 20 °C to 40 °C, we found that the core-DNA phase undergoes a density and volume transition close to the physiological temperature of infection (~37 °C). The transition yields a lower energy state of DNA in the capsid core due to lower density and reduced packing defects. This increases DNA mobility, which is required to initiate rapid genome ejection from the virus capsid into a host cell, causing infection. These data reconcile our earlier findings of mechanical DNA transition in phage.</p>}},
author = {{Villanueva Valencia, José Ramón and Tsimtsirakis, Efthymios and Krueger, Susan and Evilevitch, Alex}},
issn = {{1091-6490}},
keywords = {{Bacteriophage lambda/genetics; Capsid/chemistry; Temperature; Cryoelectron Microscopy; DNA, Viral/chemistry; Capsid Proteins/genetics}},
language = {{eng}},
month = {{11}},
number = {{45}},
publisher = {{National Academy of Sciences}},
series = {{Proceedings of the National Academy of Sciences of the United States of America}},
title = {{Temperature-induced DNA density transition in phage λ capsid revealed with contrast-matching SANS}},
url = {{http://dx.doi.org/10.1073/pnas.2220518120}},
doi = {{10.1073/pnas.2220518120}},
volume = {{120}},
year = {{2023}},
}