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A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system

DndABCDE-catalyzed DNA phosphorothioation (PT), in which the nonbridging oxygen is swapped with a sulfur atom, was first identified in the bacterial genome. Usually, this modification gene cluster is paired with a restriction module consisting of DndF, DndG, and DndH. Although the mechanisms for the...

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Autores principales: Jiang, Susu, Chen, Ke, Wang, Yingying, Zhang, Yueying, Tang, Yaru, Huang, Wanqiu, Xiong, Xiaolin, Chen, Shi, Chen, Chao, Wang, Lianrong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470545/
https://www.ncbi.nlm.nih.gov/pubmed/37260233
http://dx.doi.org/10.1128/mbio.00933-23
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author Jiang, Susu
Chen, Ke
Wang, Yingying
Zhang, Yueying
Tang, Yaru
Huang, Wanqiu
Xiong, Xiaolin
Chen, Shi
Chen, Chao
Wang, Lianrong
author_facet Jiang, Susu
Chen, Ke
Wang, Yingying
Zhang, Yueying
Tang, Yaru
Huang, Wanqiu
Xiong, Xiaolin
Chen, Shi
Chen, Chao
Wang, Lianrong
author_sort Jiang, Susu
collection PubMed
description DndABCDE-catalyzed DNA phosphorothioation (PT), in which the nonbridging oxygen is swapped with a sulfur atom, was first identified in the bacterial genome. Usually, this modification gene cluster is paired with a restriction module consisting of DndF, DndG, and DndH. Although the mechanisms for the antiphage activity conferred by this Dnd-related restriction and modification (R-M) system have been well characterized, several features remain unclear, including the antiphage spectrum and potential interference with DNA methylation. Recently, a novel PT-related R-M system, composed of the modification module SspABCD paired with a single restriction enzyme, SspE, was revealed to be widespread in the bacterial kingdom, which aroused our interest in the interaction between Dnd- and Ssp-based R-M systems. In this study, we discussed the action of Dnd-related R-M systems against phages and demonstrated that the host could benefit from the protection provided by Dnd-related R-M systems against infection by various lytic phages as well as temperate phages. However, this defense barrier would fail against lysogenic phages. Interestingly, DNA methylation, even in the consensus sequence recognized by the Dnd system, could not weaken the restriction efficiency. Finally, we explored the interaction between Dnd- and Ssp-based R-M systems and found that these two systems were compatible. This study not only expands our knowledge of Dnd-associated R-M systems but also reveals a complex interaction between different defense barriers that coexist in the cell. IMPORTANCE: Recently, we decoded the mechanism of Dnd-related R-M systems against genetic parasites. In the presence of exogenous DNA that lacks PT, the macromolecular machine consisting of DndF, DndG, and DndH undergoes conformational changes to perform DNA binding, translocation, and DNA nicking activities and scavenge the foreign DNA. However, several questions remain unanswered, including questions regarding the antiphage spectrum, potential interference by DNA methylation, and interplay with other PT-dependent R-M systems. Here, we revealed that the host could benefit from Dnd-related R-M systems for a broad range of antiphage activities, regardless of the presence of DNA methylation. Furthermore, we demonstrated that the convergence of Dnd- and Ssp-related R-M systems could confer to the host a stronger antiphage ability through the additive suppression of phage replication. This study not only deepens our understanding of PT-related defense barriers but also expands our knowledge of the arms race between bacteria and their predators.
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spelling pubmed-104705452023-09-01 A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system Jiang, Susu Chen, Ke Wang, Yingying Zhang, Yueying Tang, Yaru Huang, Wanqiu Xiong, Xiaolin Chen, Shi Chen, Chao Wang, Lianrong mBio Research Article DndABCDE-catalyzed DNA phosphorothioation (PT), in which the nonbridging oxygen is swapped with a sulfur atom, was first identified in the bacterial genome. Usually, this modification gene cluster is paired with a restriction module consisting of DndF, DndG, and DndH. Although the mechanisms for the antiphage activity conferred by this Dnd-related restriction and modification (R-M) system have been well characterized, several features remain unclear, including the antiphage spectrum and potential interference with DNA methylation. Recently, a novel PT-related R-M system, composed of the modification module SspABCD paired with a single restriction enzyme, SspE, was revealed to be widespread in the bacterial kingdom, which aroused our interest in the interaction between Dnd- and Ssp-based R-M systems. In this study, we discussed the action of Dnd-related R-M systems against phages and demonstrated that the host could benefit from the protection provided by Dnd-related R-M systems against infection by various lytic phages as well as temperate phages. However, this defense barrier would fail against lysogenic phages. Interestingly, DNA methylation, even in the consensus sequence recognized by the Dnd system, could not weaken the restriction efficiency. Finally, we explored the interaction between Dnd- and Ssp-based R-M systems and found that these two systems were compatible. This study not only expands our knowledge of Dnd-associated R-M systems but also reveals a complex interaction between different defense barriers that coexist in the cell. IMPORTANCE: Recently, we decoded the mechanism of Dnd-related R-M systems against genetic parasites. In the presence of exogenous DNA that lacks PT, the macromolecular machine consisting of DndF, DndG, and DndH undergoes conformational changes to perform DNA binding, translocation, and DNA nicking activities and scavenge the foreign DNA. However, several questions remain unanswered, including questions regarding the antiphage spectrum, potential interference by DNA methylation, and interplay with other PT-dependent R-M systems. Here, we revealed that the host could benefit from Dnd-related R-M systems for a broad range of antiphage activities, regardless of the presence of DNA methylation. Furthermore, we demonstrated that the convergence of Dnd- and Ssp-related R-M systems could confer to the host a stronger antiphage ability through the additive suppression of phage replication. This study not only deepens our understanding of PT-related defense barriers but also expands our knowledge of the arms race between bacteria and their predators. American Society for Microbiology 2023-06-01 /pmc/articles/PMC10470545/ /pubmed/37260233 http://dx.doi.org/10.1128/mbio.00933-23 Text en Copyright © 2023 Jiang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Jiang, Susu
Chen, Ke
Wang, Yingying
Zhang, Yueying
Tang, Yaru
Huang, Wanqiu
Xiong, Xiaolin
Chen, Shi
Chen, Chao
Wang, Lianrong
A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title_full A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title_fullStr A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title_full_unstemmed A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title_short A DNA phosphorothioation-based Dnd defense system provides resistance against various phages and is compatible with the Ssp defense system
title_sort dna phosphorothioation-based dnd defense system provides resistance against various phages and is compatible with the ssp defense system
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10470545/
https://www.ncbi.nlm.nih.gov/pubmed/37260233
http://dx.doi.org/10.1128/mbio.00933-23
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