Essential gene acquisition destabilizes plasmid inheritance.

Extra-chromosomal genetic elements are important drivers of evolutionary transformations and ecological adaptations in prokaryotes with their evolutionary success often depending on their 'utility' to the host. Examples are plasmids encoding antibiotic resistance genes, which are known to...

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Autores principales:	Tanita Wein, Yiqing Wang, Myriam Barz, Fenna T Stücker, Katrin Hammerschmidt, Tal Dagan
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Genetics QH426-470
Acceso en línea:	https://doaj.org/article/84466bf55e654e12aee9931abdb90bb1
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spelling	oai:doaj.org-article:84466bf55e654e12aee9931abdb90bb12021-12-02T20:02:56ZEssential gene acquisition destabilizes plasmid inheritance.1553-73901553-740410.1371/journal.pgen.1009656https://doaj.org/article/84466bf55e654e12aee9931abdb90bb12021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009656https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Extra-chromosomal genetic elements are important drivers of evolutionary transformations and ecological adaptations in prokaryotes with their evolutionary success often depending on their 'utility' to the host. Examples are plasmids encoding antibiotic resistance genes, which are known to proliferate in the presence of antibiotics. Plasmids carrying an essential host function are recognized as permanent residents in their host. Essential plasmids have been reported in several taxa where they often encode essential metabolic functions; nonetheless, their evolution remains poorly understood. Here we show that essential genes are rarely encoded on plasmids; evolving essential plasmids in Escherichia coli we further find that acquisition of an essential chromosomal gene by a plasmid can lead to plasmid extinction. A comparative genomics analysis of Escherichia isolates reveals few plasmid-encoded essential genes, yet these are often integrated into plasmid-related functions; an example is the GroEL/GroES chaperonin. Experimental evolution of a chaperonin-encoding plasmid shows that the acquisition of an essential gene reduces plasmid fitness regardless of the stability of plasmid inheritance. Our results suggest that essential plasmid emergence leads to a dose effect caused by gene redundancy. The detrimental effect of essential gene acquisition on plasmid inheritance constitutes a barrier for plasmid-mediated lateral gene transfer and supplies a mechanistic understanding for the rarity of essential genes in extra-chromosomal genetic elements.Tanita WeinYiqing WangMyriam BarzFenna T StückerKatrin HammerschmidtTal DaganPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 7, p e1009656 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Genetics QH426-470
spellingShingle	Genetics QH426-470 Tanita Wein Yiqing Wang Myriam Barz Fenna T Stücker Katrin Hammerschmidt Tal Dagan Essential gene acquisition destabilizes plasmid inheritance.
description	Extra-chromosomal genetic elements are important drivers of evolutionary transformations and ecological adaptations in prokaryotes with their evolutionary success often depending on their 'utility' to the host. Examples are plasmids encoding antibiotic resistance genes, which are known to proliferate in the presence of antibiotics. Plasmids carrying an essential host function are recognized as permanent residents in their host. Essential plasmids have been reported in several taxa where they often encode essential metabolic functions; nonetheless, their evolution remains poorly understood. Here we show that essential genes are rarely encoded on plasmids; evolving essential plasmids in Escherichia coli we further find that acquisition of an essential chromosomal gene by a plasmid can lead to plasmid extinction. A comparative genomics analysis of Escherichia isolates reveals few plasmid-encoded essential genes, yet these are often integrated into plasmid-related functions; an example is the GroEL/GroES chaperonin. Experimental evolution of a chaperonin-encoding plasmid shows that the acquisition of an essential gene reduces plasmid fitness regardless of the stability of plasmid inheritance. Our results suggest that essential plasmid emergence leads to a dose effect caused by gene redundancy. The detrimental effect of essential gene acquisition on plasmid inheritance constitutes a barrier for plasmid-mediated lateral gene transfer and supplies a mechanistic understanding for the rarity of essential genes in extra-chromosomal genetic elements.
format	article
author	Tanita Wein Yiqing Wang Myriam Barz Fenna T Stücker Katrin Hammerschmidt Tal Dagan
author_facet	Tanita Wein Yiqing Wang Myriam Barz Fenna T Stücker Katrin Hammerschmidt Tal Dagan
author_sort	Tanita Wein
title	Essential gene acquisition destabilizes plasmid inheritance.
title_short	Essential gene acquisition destabilizes plasmid inheritance.
title_full	Essential gene acquisition destabilizes plasmid inheritance.
title_fullStr	Essential gene acquisition destabilizes plasmid inheritance.
title_full_unstemmed	Essential gene acquisition destabilizes plasmid inheritance.
title_sort	essential gene acquisition destabilizes plasmid inheritance.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/84466bf55e654e12aee9931abdb90bb1
work_keys_str_mv	AT tanitawein essentialgeneacquisitiondestabilizesplasmidinheritance AT yiqingwang essentialgeneacquisitiondestabilizesplasmidinheritance AT myriambarz essentialgeneacquisitiondestabilizesplasmidinheritance AT fennatstucker essentialgeneacquisitiondestabilizesplasmidinheritance AT katrinhammerschmidt essentialgeneacquisitiondestabilizesplasmidinheritance AT taldagan essentialgeneacquisitiondestabilizesplasmidinheritance
_version_	1718375670437904384

Essential gene acquisition destabilizes plasmid inheritance.

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