Re-wiring of energy metabolism promotes viability during hyperreplication stress in E. coli

Godefroid Charbon; Christopher Campion; Siu Hung Joshua Chan; Louise Bjørn; Allan Weimann; Luís Cláudio Nascimento da Silva; Peter Ruhdal Jensen; Anders Løbner-Olesen

doi:10.1371/journal.pgen.1006590

Re-wiring of energy metabolism promotes viability during hyperreplication stress in E. coli

Godefroid Charbon, Christopher Campion, Siu Hung Joshua Chan, Louise Bjørn, Allan Weimann, Luís Cláudio Nascimento da Silva, Peter Ruhdal Jensen, Anders Løbner-Olesen

Functional genomics

14 Citationer (Scopus)

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Abstract

Chromosome replication in Escherichia coli is initiated by DnaA. DnaA binds ATP which is essential for formation of a DnaA-oriC nucleoprotein complex that promotes strand opening, helicase loading and replisome assembly. Following initiation, DnaAATP is converted to DnaAADP primarily by the Regulatory Inactivation of DnaA process (RIDA). In RIDA deficient cells, DnaAATP accumulates leading to uncontrolled initiation of replication and cell death by accumulation of DNA strand breaks. Mutations that suppress RIDA deficiency either dampen overinitiation or permit growth despite overinitiation. We characterize mutations of the last group that have in common that distinct metabolic routes are rewired resulting in the redirection of electron flow towards the cytochrome bd-1. We propose a model where cytochrome bd-1 lowers the formation of reactive oxygen species and hence oxidative damage to the DNA in general. This increases the processivity of replication forks generated by overinitiation to a level that sustains viability.

Originalsprog	Engelsk
Artikelnummer	e1006590
Tidsskrift	PLoS Genetics
Vol/bind	13
Udgave nummer	1
Antal sider	26
ISSN	1553-7390
DOI	https://doi.org/10.1371/journal.pgen.1006590
Status	Udgivet - 27 jan. 2017

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10.1371/journal.pgen.1006590Licens: CC BY

Charbon_2017_Re-wiring_of_energyForlagets udgivne version, 5,98 MBLicens: CC BY

Citationsformater

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abstract = "Chromosome replication in Escherichia coli is initiated by DnaA. DnaA binds ATP which is essential for formation of a DnaA-oriC nucleoprotein complex that promotes strand opening, helicase loading and replisome assembly. Following initiation, DnaAATP is converted to DnaAADP primarily by the Regulatory Inactivation of DnaA process (RIDA). In RIDA deficient cells, DnaAATP accumulates leading to uncontrolled initiation of replication and cell death by accumulation of DNA strand breaks. Mutations that suppress RIDA deficiency either dampen overinitiation or permit growth despite overinitiation. We characterize mutations of the last group that have in common that distinct metabolic routes are rewired resulting in the redirection of electron flow towards the cytochrome bd-1. We propose a model where cytochrome bd-1 lowers the formation of reactive oxygen species and hence oxidative damage to the DNA in general. This increases the processivity of replication forks generated by overinitiation to a level that sustains viability.",

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T1 - Re-wiring of energy metabolism promotes viability during hyperreplication stress in E. coli

AU - Charbon, Godefroid

AU - Campion, Christopher

AU - Chan, Siu Hung Joshua

AU - Bjørn, Louise

AU - Weimann, Allan

AU - da Silva, Luís Cláudio Nascimento

AU - Jensen, Peter Ruhdal

AU - Løbner-Olesen, Anders

PY - 2017/1/27

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N2 - Chromosome replication in Escherichia coli is initiated by DnaA. DnaA binds ATP which is essential for formation of a DnaA-oriC nucleoprotein complex that promotes strand opening, helicase loading and replisome assembly. Following initiation, DnaAATP is converted to DnaAADP primarily by the Regulatory Inactivation of DnaA process (RIDA). In RIDA deficient cells, DnaAATP accumulates leading to uncontrolled initiation of replication and cell death by accumulation of DNA strand breaks. Mutations that suppress RIDA deficiency either dampen overinitiation or permit growth despite overinitiation. We characterize mutations of the last group that have in common that distinct metabolic routes are rewired resulting in the redirection of electron flow towards the cytochrome bd-1. We propose a model where cytochrome bd-1 lowers the formation of reactive oxygen species and hence oxidative damage to the DNA in general. This increases the processivity of replication forks generated by overinitiation to a level that sustains viability.

AB - Chromosome replication in Escherichia coli is initiated by DnaA. DnaA binds ATP which is essential for formation of a DnaA-oriC nucleoprotein complex that promotes strand opening, helicase loading and replisome assembly. Following initiation, DnaAATP is converted to DnaAADP primarily by the Regulatory Inactivation of DnaA process (RIDA). In RIDA deficient cells, DnaAATP accumulates leading to uncontrolled initiation of replication and cell death by accumulation of DNA strand breaks. Mutations that suppress RIDA deficiency either dampen overinitiation or permit growth despite overinitiation. We characterize mutations of the last group that have in common that distinct metabolic routes are rewired resulting in the redirection of electron flow towards the cytochrome bd-1. We propose a model where cytochrome bd-1 lowers the formation of reactive oxygen species and hence oxidative damage to the DNA in general. This increases the processivity of replication forks generated by overinitiation to a level that sustains viability.

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DO - 10.1371/journal.pgen.1006590

M3 - Journal article

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SN - 1553-7390

VL - 13

JO - P L o S Genetics

JF - P L o S Genetics

IS - 1

M1 - e1006590

ER -

Re-wiring of energy metabolism promotes viability during hyperreplication stress in E. coli

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