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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eLife Sciences Publications Ltd
2017-10-01
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Series: | eLife |
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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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institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T02:01:18Z |
publishDate | 2017-10-01 |
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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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