Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system

ABSTRACTBacteria have developed various defense mechanisms against phages. Abortive infection (Abi), a bacterial defense mechanism, can be achieved through various means, including toxin-antitoxin systems, cyclic oligonucleotide-based antiphage signaling systems, and retrons. AbpA and AbpB (AbpAB) d...

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Main Authors: Takaomi Sasaki, Saya Takita, Takashi Fujishiro, Yunosuke Shintani, Satoki Nojiri, Ryota Yasui, Tetsuro Yonesaki, Yuichi Otsuka
Format: Article
Language:English
Published: American Society for Microbiology 2023-12-01
Series:mSphere
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msphere.00372-23
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author Takaomi Sasaki
Saya Takita
Takashi Fujishiro
Yunosuke Shintani
Satoki Nojiri
Ryota Yasui
Tetsuro Yonesaki
Yuichi Otsuka
author_facet Takaomi Sasaki
Saya Takita
Takashi Fujishiro
Yunosuke Shintani
Satoki Nojiri
Ryota Yasui
Tetsuro Yonesaki
Yuichi Otsuka
author_sort Takaomi Sasaki
collection DOAJ
description ABSTRACTBacteria have developed various defense mechanisms against phages. Abortive infection (Abi), a bacterial defense mechanism, can be achieved through various means, including toxin-antitoxin systems, cyclic oligonucleotide-based antiphage signaling systems, and retrons. AbpA and AbpB (AbpAB) defend against many lytic phages harboring double-stranded DNA genomes in Escherichia coli; however, how AbpAB senses phage infection and inhibits its propagation remains unclear. Here, we demonstrated that AbpAB inhibited the growth of the φX174 lytic phage with single-stranded DNA (ssDNA) as well as the lysogenization and induction of the Sakai prophage 5 lysogenic phage. The AbpAB defense system limits T4 and φX174 phage propagation via Abi. AbpA contains a nuclease domain at its N-terminus, and AbpB has an ATP-dependent RNA helicase domain; both domains are required for phage defense. This system is activated by phage Gp32 binding to ssDNA and inhibits E. coli growth. Without phage infection, DNA replication inhibitors or defects in the DNA repair factors RecB and RecC activate this system. Therefore, the E. coli AbpAB defense system may sense DNA-protein complexes, including the phage-encoded ssDNA-binding protein or those formed by interrupting host DNA replication or repair.IMPORTANCEAlthough numerous phage defense systems have recently been discovered in bacteria, how these systems defend against phage propagation or sense phage infections remains unclear. The Escherichia coli AbpAB defense system targets several lytic and lysogenic phages harboring DNA genomes. A phage-encoded single-stranded DNA-binding protein, Gp32, activates this system similar to other phage defense systems such as Retron-Eco8, Hachiman, ShosTA, Nhi, and Hna. DNA replication inhibitors or defects in DNA repair factors activate the AbpAB system, even without phage infection. This is one of the few examples of activating phage defense systems without phage infection or proteins. The AbpAB defense system may be activated by sensing specific DNA-protein complexes.
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spelling doaj.art-84a387e9d8c349f28cdfd39c8348892b2023-12-20T14:01:03ZengAmerican Society for MicrobiologymSphere2379-50422023-12-018610.1128/msphere.00372-23Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense systemTakaomi Sasaki0Saya Takita1Takashi Fujishiro2Yunosuke Shintani3Satoki Nojiri4Ryota Yasui5Tetsuro Yonesaki6Yuichi Otsuka7Department of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanDepartment of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanDepartment of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanDepartment of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanDepartment of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Osaka, JapanDepartment of Biological Sciences, Graduate School of Science, Osaka University, Osaka, JapanDepartment of Biochemistry and Molecular Biology, Graduate School of Science and Engineering, Saitama University, Saitama, JapanABSTRACTBacteria have developed various defense mechanisms against phages. Abortive infection (Abi), a bacterial defense mechanism, can be achieved through various means, including toxin-antitoxin systems, cyclic oligonucleotide-based antiphage signaling systems, and retrons. AbpA and AbpB (AbpAB) defend against many lytic phages harboring double-stranded DNA genomes in Escherichia coli; however, how AbpAB senses phage infection and inhibits its propagation remains unclear. Here, we demonstrated that AbpAB inhibited the growth of the φX174 lytic phage with single-stranded DNA (ssDNA) as well as the lysogenization and induction of the Sakai prophage 5 lysogenic phage. The AbpAB defense system limits T4 and φX174 phage propagation via Abi. AbpA contains a nuclease domain at its N-terminus, and AbpB has an ATP-dependent RNA helicase domain; both domains are required for phage defense. This system is activated by phage Gp32 binding to ssDNA and inhibits E. coli growth. Without phage infection, DNA replication inhibitors or defects in the DNA repair factors RecB and RecC activate this system. Therefore, the E. coli AbpAB defense system may sense DNA-protein complexes, including the phage-encoded ssDNA-binding protein or those formed by interrupting host DNA replication or repair.IMPORTANCEAlthough numerous phage defense systems have recently been discovered in bacteria, how these systems defend against phage propagation or sense phage infections remains unclear. The Escherichia coli AbpAB defense system targets several lytic and lysogenic phages harboring DNA genomes. A phage-encoded single-stranded DNA-binding protein, Gp32, activates this system similar to other phage defense systems such as Retron-Eco8, Hachiman, ShosTA, Nhi, and Hna. DNA replication inhibitors or defects in DNA repair factors activate the AbpAB system, even without phage infection. This is one of the few examples of activating phage defense systems without phage infection or proteins. The AbpAB defense system may be activated by sensing specific DNA-protein complexes.https://journals.asm.org/doi/10.1128/msphere.00372-23bacteriophagesEscherichia coliphage defense systemAbpA-AbpB
spellingShingle Takaomi Sasaki
Saya Takita
Takashi Fujishiro
Yunosuke Shintani
Satoki Nojiri
Ryota Yasui
Tetsuro Yonesaki
Yuichi Otsuka
Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
mSphere
bacteriophages
Escherichia coli
phage defense system
AbpA-AbpB
title Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
title_full Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
title_fullStr Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
title_full_unstemmed Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
title_short Phage single-stranded DNA-binding protein or host DNA damage triggers the activation of the AbpAB phage defense system
title_sort phage single stranded dna binding protein or host dna damage triggers the activation of the abpab phage defense system
topic bacteriophages
Escherichia coli
phage defense system
AbpA-AbpB
url https://journals.asm.org/doi/10.1128/msphere.00372-23
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