Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands

Staphylococcus aureus pathogenicity islands (SaPIs), such as SaPI1, exploit specific helper bacteriophages, like 80α, for their high frequency mobilization, a process termed ‘molecular piracy’. SaPI1 redirects the helper’s assembly pathway to form small capsids that can only accommodate the smaller...

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Main Authors: Altaira D Dearborn, Erin A Wall, James L Kizziah, Laura Klenow, Laura K Parker, Keith A Manning, Michael S Spilman, John M Spear, Gail E Christie, Terje Dokland
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/30822
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author Altaira D Dearborn
Erin A Wall
James L Kizziah
Laura Klenow
Laura K Parker
Keith A Manning
Michael S Spilman
John M Spear
Gail E Christie
Terje Dokland
author_facet Altaira D Dearborn
Erin A Wall
James L Kizziah
Laura Klenow
Laura K Parker
Keith A Manning
Michael S Spilman
John M Spear
Gail E Christie
Terje Dokland
author_sort Altaira D Dearborn
collection DOAJ
description Staphylococcus aureus pathogenicity islands (SaPIs), such as SaPI1, exploit specific helper bacteriophages, like 80α, for their high frequency mobilization, a process termed ‘molecular piracy’. SaPI1 redirects the helper’s assembly pathway to form small capsids that can only accommodate the smaller SaPI1 genome, but not a complete phage genome. SaPI1 encodes two proteins, CpmA and CpmB, that are responsible for this size redirection. We have determined the structures of the 80α and SaPI1 procapsids to near-atomic resolution by cryo-electron microscopy, and show that CpmB competes with the 80α scaffolding protein (SP) for a binding site on the capsid protein (CP), and works by altering the angle between capsomers. We probed these interactions genetically and identified second-site suppressors of lethal mutations in SP. Our structures show, for the first time, the detailed interactions between SP and CP in a bacteriophage, providing unique insights into macromolecular assembly processes.
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spelling doaj.art-72076c0e1d274158af0e53f40362b9e12022-12-22T03:52:40ZengeLife Sciences Publications LtdeLife2050-084X2017-10-01610.7554/eLife.30822Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islandsAltaira D Dearborn0Erin A Wall1James L Kizziah2Laura Klenow3Laura K Parker4Keith A Manning5Michael S Spilman6John M Spear7Gail E Christie8Terje Dokland9https://orcid.org/0000-0001-5655-4123Protein Expression Laboratory, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, United StatesDepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United StatesDepartment of Microbiology, University of Alabama, Birmingham, United StatesDepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United StatesDepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United States; Department of Microbiology, University of Alabama, Birmingham, United StatesDepartment of Microbiology, University of Alabama, Birmingham, United StatesDirect Electron, San Diego, United StatesBiological Science Imaging Resource, Florida State University, Tallahassee, United StatesDepartment of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United StatesDepartment of Microbiology, University of Alabama, Birmingham, United StatesStaphylococcus aureus pathogenicity islands (SaPIs), such as SaPI1, exploit specific helper bacteriophages, like 80α, for their high frequency mobilization, a process termed ‘molecular piracy’. SaPI1 redirects the helper’s assembly pathway to form small capsids that can only accommodate the smaller SaPI1 genome, but not a complete phage genome. SaPI1 encodes two proteins, CpmA and CpmB, that are responsible for this size redirection. We have determined the structures of the 80α and SaPI1 procapsids to near-atomic resolution by cryo-electron microscopy, and show that CpmB competes with the 80α scaffolding protein (SP) for a binding site on the capsid protein (CP), and works by altering the angle between capsomers. We probed these interactions genetically and identified second-site suppressors of lethal mutations in SP. Our structures show, for the first time, the detailed interactions between SP and CP in a bacteriophage, providing unique insights into macromolecular assembly processes.https://elifesciences.org/articles/30822bacteriophage 80alphaS. aureus pathogenicity island 1 (SaPI1)cryo-electron microscopyvirus structure and assemblythree-dimensional reconstructionStaphylococcus aureus
spellingShingle Altaira D Dearborn
Erin A Wall
James L Kizziah
Laura Klenow
Laura K Parker
Keith A Manning
Michael S Spilman
John M Spear
Gail E Christie
Terje Dokland
Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
eLife
bacteriophage 80alpha
S. aureus pathogenicity island 1 (SaPI1)
cryo-electron microscopy
virus structure and assembly
three-dimensional reconstruction
Staphylococcus aureus
title Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
title_full Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
title_fullStr Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
title_full_unstemmed Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
title_short Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
title_sort competing scaffolding proteins determine capsid size during mobilization of staphylococcus aureus pathogenicity islands
topic bacteriophage 80alpha
S. aureus pathogenicity island 1 (SaPI1)
cryo-electron microscopy
virus structure and assembly
three-dimensional reconstruction
Staphylococcus aureus
url https://elifesciences.org/articles/30822
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