Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs

ABSTRACT Genes encoding proteins that carry out essential informational tasks in the cell, in particular where multiple interaction partners are involved, are less likely to be transferable to a foreign organism. Here, we investigated the constraints on transfer of a gene encoding a highly conserved...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Betül Kacar, Eva Garmendia, Nurcan Tuncbag, Dan I. Andersson, Diarmaid Hughes
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	EF-Tu horizontal gene transfer ancient genes proteobacteria tuf Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ab92cac42b6242cc93fa6068610121f7
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:ab92cac42b6242cc93fa6068610121f7
record_format	dspace
spelling	oai:doaj.org-article:ab92cac42b6242cc93fa6068610121f72021-11-15T15:51:43ZFunctional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs10.1128/mBio.01276-172150-7511https://doaj.org/article/ab92cac42b6242cc93fa6068610121f72017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01276-17https://doaj.org/toc/2150-7511ABSTRACT Genes encoding proteins that carry out essential informational tasks in the cell, in particular where multiple interaction partners are involved, are less likely to be transferable to a foreign organism. Here, we investigated the constraints on transfer of a gene encoding a highly conserved informational protein, translation elongation factor Tu (EF-Tu), by systematically replacing the endogenous tufA gene in the Escherichia coli genome with its extant and ancestral homologs. The extant homologs represented tuf variants from both near and distant homologous organisms. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 billion years ago (bya). Our results demonstrate that all of the foreign tuf genes are transferable to the E. coli genome, provided that an additional copy of the EF-Tu gene, tufB, remains present in the E. coli genome. However, when the tufB gene was removed, only the variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth which demonstrates the limited functional interchangeability of E. coli tuf with its homologs. Relative bacterial fitness correlated with the evolutionary distance of the extant tuf homologs inserted into the E. coli genome. This reduced fitness was associated with reduced levels of EF-Tu and reduced rates of protein synthesis. Increasing the expression of tuf partially ameliorated these fitness costs. In summary, our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria. IMPORTANCE Horizontal gene transfer (HGT) is a fundamental driving force in bacterial evolution. However, whether essential genes can be acquired by HGT and whether they can be acquired from distant organisms are very poorly understood. By systematically replacing tuf with ancestral homologs and homologs from distantly related organisms, we investigated the constraints on HGT of a highly conserved gene with multiple interaction partners. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 bya. Only variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth, demonstrating the limited functional interchangeability of E. coli tuf with its homologs. Our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria.Betül KacarEva GarmendiaNurcan TuncbagDan I. AnderssonDiarmaid HughesAmerican Society for MicrobiologyarticleEF-Tuhorizontal gene transferancient genesproteobacteriatufMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	EF-Tu horizontal gene transfer ancient genes proteobacteria tuf Microbiology QR1-502
spellingShingle	EF-Tu horizontal gene transfer ancient genes proteobacteria tuf Microbiology QR1-502 Betül Kacar Eva Garmendia Nurcan Tuncbag Dan I. Andersson Diarmaid Hughes Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
description	ABSTRACT Genes encoding proteins that carry out essential informational tasks in the cell, in particular where multiple interaction partners are involved, are less likely to be transferable to a foreign organism. Here, we investigated the constraints on transfer of a gene encoding a highly conserved informational protein, translation elongation factor Tu (EF-Tu), by systematically replacing the endogenous tufA gene in the Escherichia coli genome with its extant and ancestral homologs. The extant homologs represented tuf variants from both near and distant homologous organisms. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 billion years ago (bya). Our results demonstrate that all of the foreign tuf genes are transferable to the E. coli genome, provided that an additional copy of the EF-Tu gene, tufB, remains present in the E. coli genome. However, when the tufB gene was removed, only the variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth which demonstrates the limited functional interchangeability of E. coli tuf with its homologs. Relative bacterial fitness correlated with the evolutionary distance of the extant tuf homologs inserted into the E. coli genome. This reduced fitness was associated with reduced levels of EF-Tu and reduced rates of protein synthesis. Increasing the expression of tuf partially ameliorated these fitness costs. In summary, our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria. IMPORTANCE Horizontal gene transfer (HGT) is a fundamental driving force in bacterial evolution. However, whether essential genes can be acquired by HGT and whether they can be acquired from distant organisms are very poorly understood. By systematically replacing tuf with ancestral homologs and homologs from distantly related organisms, we investigated the constraints on HGT of a highly conserved gene with multiple interaction partners. The ancestral homologs represented phylogenetically resurrected tuf sequences dating from 0.7 to 3.6 bya. Only variants obtained from the gammaproteobacterial family (extant and ancestral) supported growth, demonstrating the limited functional interchangeability of E. coli tuf with its homologs. Our analysis suggests that the functional conservation of protein activity, the amount of protein expressed, and its network connectivity act to constrain the successful transfer of this essential gene into foreign bacteria.
format	article
author	Betül Kacar Eva Garmendia Nurcan Tuncbag Dan I. Andersson Diarmaid Hughes
author_facet	Betül Kacar Eva Garmendia Nurcan Tuncbag Dan I. Andersson Diarmaid Hughes
author_sort	Betül Kacar
title	Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
title_short	Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
title_full	Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
title_fullStr	Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
title_full_unstemmed	Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs
title_sort	functional constraints on replacing an essential gene with its ancient and modern homologs
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/ab92cac42b6242cc93fa6068610121f7
work_keys_str_mv	AT betulkacar functionalconstraintsonreplacinganessentialgenewithitsancientandmodernhomologs AT evagarmendia functionalconstraintsonreplacinganessentialgenewithitsancientandmodernhomologs AT nurcantuncbag functionalconstraintsonreplacinganessentialgenewithitsancientandmodernhomologs AT daniandersson functionalconstraintsonreplacinganessentialgenewithitsancientandmodernhomologs AT diarmaidhughes functionalconstraintsonreplacinganessentialgenewithitsancientandmodernhomologs
_version_	1718427359699271680

Functional Constraints on Replacing an Essential Gene with Its Ancient and Modern Homologs

Ejemplares similares