Thermus thermophilus Argonaute Functions in the Completion of DNA Replication

Samson M. Jolly; Ildar Gainetdinov; Karina Jouravleva; Han Zhang; Lara Strittmatter; Shannon M. Bailey; Gregory M. Hendricks; Avantika Dhabaria; Beatrix Ueberheide; Phillip D. Zamore

doi:10.1016/j.cell.2020.07.036

Thermus thermophilus Argonaute Functions in the Completion of DNA Replication

Samson M. Jolly, Ildar Gainetdinov, Karina Jouravleva, Han Zhang, Lara Strittmatter, Shannon M. Bailey, Gregory M. Hendricks, Avantika Dhabaria, Beatrix Ueberheide, Phillip D. Zamore

Biology and Genomics

Research output: Contribution to journal › Article › peer-review

Abstract

In many eukaryotes, Argonaute proteins, guided by short RNA sequences, defend cells against transposons and viruses. In the eubacterium Thermus thermophilus, the DNA-guided Argonaute TtAgo defends against transformation by DNA plasmids. Here, we report that TtAgo also participates in DNA replication. In vivo, TtAgo binds 15- to 18-nt DNA guides derived from the chromosomal region where replication terminates and associates with proteins known to act in DNA replication. When gyrase, the sole T. thermophilus type II topoisomerase, is inhibited, TtAgo allows the bacterium to finish replicating its circular genome. In contrast, loss of gyrase and TtAgo activity slows growth and produces long sausage-like filaments in which the individual bacteria are linked by DNA. Finally, wild-type T. thermophilus outcompetes an otherwise isogenic strain lacking TtAgo. We propose that the primary role of TtAgo is to help T. thermophilus disentangle the catenated circular chromosomes generated by DNA replication.

Original language	English (US)
Pages (from-to)	1545-1559.e18
Journal	Cell
Volume	182
Issue number	6
DOIs	https://doi.org/10.1016/j.cell.2020.07.036
State	Published - Sep 17 2020

Keywords

Argonaute
DNA replication
RNA silencing
Thermus thermophilus
TtAgo
decatenation
gyrase
pAGO
terminus of replication
topoisomerase

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2020.07.036

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title = "Thermus thermophilus Argonaute Functions in the Completion of DNA Replication",

abstract = "In many eukaryotes, Argonaute proteins, guided by short RNA sequences, defend cells against transposons and viruses. In the eubacterium Thermus thermophilus, the DNA-guided Argonaute TtAgo defends against transformation by DNA plasmids. Here, we report that TtAgo also participates in DNA replication. In vivo, TtAgo binds 15- to 18-nt DNA guides derived from the chromosomal region where replication terminates and associates with proteins known to act in DNA replication. When gyrase, the sole T. thermophilus type II topoisomerase, is inhibited, TtAgo allows the bacterium to finish replicating its circular genome. In contrast, loss of gyrase and TtAgo activity slows growth and produces long sausage-like filaments in which the individual bacteria are linked by DNA. Finally, wild-type T. thermophilus outcompetes an otherwise isogenic strain lacking TtAgo. We propose that the primary role of TtAgo is to help T. thermophilus disentangle the catenated circular chromosomes generated by DNA replication.",

keywords = "Argonaute, DNA replication, RNA silencing, Thermus thermophilus, TtAgo, decatenation, gyrase, pAGO, terminus of replication, topoisomerase",

author = "Jolly, {Samson M.} and Ildar Gainetdinov and Karina Jouravleva and Han Zhang and Lara Strittmatter and Bailey, {Shannon M.} and Hendricks, {Gregory M.} and Avantika Dhabaria and Beatrix Ueberheide and Zamore, {Phillip D.}",

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T1 - Thermus thermophilus Argonaute Functions in the Completion of DNA Replication

AU - Jolly, Samson M.

AU - Gainetdinov, Ildar

AU - Jouravleva, Karina

AU - Zhang, Han

AU - Strittmatter, Lara

AU - Bailey, Shannon M.

AU - Hendricks, Gregory M.

AU - Dhabaria, Avantika

AU - Ueberheide, Beatrix

AU - Zamore, Phillip D.

PY - 2020/9/17

Y1 - 2020/9/17

N2 - In many eukaryotes, Argonaute proteins, guided by short RNA sequences, defend cells against transposons and viruses. In the eubacterium Thermus thermophilus, the DNA-guided Argonaute TtAgo defends against transformation by DNA plasmids. Here, we report that TtAgo also participates in DNA replication. In vivo, TtAgo binds 15- to 18-nt DNA guides derived from the chromosomal region where replication terminates and associates with proteins known to act in DNA replication. When gyrase, the sole T. thermophilus type II topoisomerase, is inhibited, TtAgo allows the bacterium to finish replicating its circular genome. In contrast, loss of gyrase and TtAgo activity slows growth and produces long sausage-like filaments in which the individual bacteria are linked by DNA. Finally, wild-type T. thermophilus outcompetes an otherwise isogenic strain lacking TtAgo. We propose that the primary role of TtAgo is to help T. thermophilus disentangle the catenated circular chromosomes generated by DNA replication.

AB - In many eukaryotes, Argonaute proteins, guided by short RNA sequences, defend cells against transposons and viruses. In the eubacterium Thermus thermophilus, the DNA-guided Argonaute TtAgo defends against transformation by DNA plasmids. Here, we report that TtAgo also participates in DNA replication. In vivo, TtAgo binds 15- to 18-nt DNA guides derived from the chromosomal region where replication terminates and associates with proteins known to act in DNA replication. When gyrase, the sole T. thermophilus type II topoisomerase, is inhibited, TtAgo allows the bacterium to finish replicating its circular genome. In contrast, loss of gyrase and TtAgo activity slows growth and produces long sausage-like filaments in which the individual bacteria are linked by DNA. Finally, wild-type T. thermophilus outcompetes an otherwise isogenic strain lacking TtAgo. We propose that the primary role of TtAgo is to help T. thermophilus disentangle the catenated circular chromosomes generated by DNA replication.

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KW - pAGO

KW - terminus of replication

KW - topoisomerase

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Thermus thermophilus Argonaute Functions in the Completion of DNA Replication

Abstract

Keywords

ASJC Scopus subject areas

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