Origins and Molecular Evolution of the NusG Paralog RfaH

ABSTRACT The only universally conserved family of transcription factors comprises housekeeping regulators and their specialized paralogs, represented by well-studied NusG and RfaH. Despite their ubiquity, little information is available on the evolutionary origins, functions, and gene targets of the...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Bing Wang, Vadim M. Gumerov, Ekaterina P. Andrianova, Igor B. Zhulin, Irina Artsimovitch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	NusG RfaH Spt5 antitermination transcription Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/32768a3b208340efa1e37e8b13041b6b
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:32768a3b208340efa1e37e8b13041b6b
record_format	dspace
spelling	oai:doaj.org-article:32768a3b208340efa1e37e8b13041b6b2021-11-15T16:19:09ZOrigins and Molecular Evolution of the NusG Paralog RfaH10.1128/mBio.02717-202150-7511https://doaj.org/article/32768a3b208340efa1e37e8b13041b6b2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02717-20https://doaj.org/toc/2150-7511ABSTRACT The only universally conserved family of transcription factors comprises housekeeping regulators and their specialized paralogs, represented by well-studied NusG and RfaH. Despite their ubiquity, little information is available on the evolutionary origins, functions, and gene targets of the NusG family members. We built a hidden Markov model profile of RfaH and identified its homologs in sequenced genomes. While NusG is widespread among bacterial phyla and coresides with genes encoding RNA polymerase and ribosome in all except extremely reduced genomes, RfaH is mostly limited to Proteobacteria and lacks common gene neighbors. RfaH activates only a few xenogeneic operons that are otherwise silenced by NusG and Rho. Phylogenetic reconstructions reveal extensive duplications and horizontal transfer of rfaH genes, including those borne by plasmids, and the molecular evolution pathway of RfaH, from “early” exclusion of the Rho terminator and tightened RNA polymerase binding to “late” interactions with the ops DNA element and autoinhibition, which together define the RfaH regulon. Remarkably, NusG is not only ubiquitous in Bacteria but also common in plants, where it likely modulates the transcription of plastid genes. IMPORTANCE In all domains of life, NusG-like proteins make contacts similar to those of RNA polymerase and promote pause-free transcription yet may play different roles, defined by their divergent interactions with nucleic acids and accessory proteins, in the same cell. This duality is illustrated by Escherichia coli NusG and RfaH, which silence and activate xenogenes, respectively. We combined sequence analysis and recent functional and structural insights to envision the evolutionary transformation of NusG, a core regulator that we show is present in all cells using bacterial RNA polymerase, into a virulence factor, RfaH. Our results suggest a stepwise conversion of a NusG duplicate copy into a sequence-specific regulator which excludes NusG from its targets but does not compromise the regulation of housekeeping genes. We find that gene duplication and lateral transfer give rise to a surprising diversity within the only ubiquitous family of transcription factors.Bing WangVadim M. GumerovEkaterina P. AndrianovaIgor B. ZhulinIrina ArtsimovitchAmerican Society for MicrobiologyarticleNusGRfaHSpt5antiterminationtranscriptionMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	NusG RfaH Spt5 antitermination transcription Microbiology QR1-502
spellingShingle	NusG RfaH Spt5 antitermination transcription Microbiology QR1-502 Bing Wang Vadim M. Gumerov Ekaterina P. Andrianova Igor B. Zhulin Irina Artsimovitch Origins and Molecular Evolution of the NusG Paralog RfaH
description	ABSTRACT The only universally conserved family of transcription factors comprises housekeeping regulators and their specialized paralogs, represented by well-studied NusG and RfaH. Despite their ubiquity, little information is available on the evolutionary origins, functions, and gene targets of the NusG family members. We built a hidden Markov model profile of RfaH and identified its homologs in sequenced genomes. While NusG is widespread among bacterial phyla and coresides with genes encoding RNA polymerase and ribosome in all except extremely reduced genomes, RfaH is mostly limited to Proteobacteria and lacks common gene neighbors. RfaH activates only a few xenogeneic operons that are otherwise silenced by NusG and Rho. Phylogenetic reconstructions reveal extensive duplications and horizontal transfer of rfaH genes, including those borne by plasmids, and the molecular evolution pathway of RfaH, from “early” exclusion of the Rho terminator and tightened RNA polymerase binding to “late” interactions with the ops DNA element and autoinhibition, which together define the RfaH regulon. Remarkably, NusG is not only ubiquitous in Bacteria but also common in plants, where it likely modulates the transcription of plastid genes. IMPORTANCE In all domains of life, NusG-like proteins make contacts similar to those of RNA polymerase and promote pause-free transcription yet may play different roles, defined by their divergent interactions with nucleic acids and accessory proteins, in the same cell. This duality is illustrated by Escherichia coli NusG and RfaH, which silence and activate xenogenes, respectively. We combined sequence analysis and recent functional and structural insights to envision the evolutionary transformation of NusG, a core regulator that we show is present in all cells using bacterial RNA polymerase, into a virulence factor, RfaH. Our results suggest a stepwise conversion of a NusG duplicate copy into a sequence-specific regulator which excludes NusG from its targets but does not compromise the regulation of housekeeping genes. We find that gene duplication and lateral transfer give rise to a surprising diversity within the only ubiquitous family of transcription factors.
format	article
author	Bing Wang Vadim M. Gumerov Ekaterina P. Andrianova Igor B. Zhulin Irina Artsimovitch
author_facet	Bing Wang Vadim M. Gumerov Ekaterina P. Andrianova Igor B. Zhulin Irina Artsimovitch
author_sort	Bing Wang
title	Origins and Molecular Evolution of the NusG Paralog RfaH
title_short	Origins and Molecular Evolution of the NusG Paralog RfaH
title_full	Origins and Molecular Evolution of the NusG Paralog RfaH
title_fullStr	Origins and Molecular Evolution of the NusG Paralog RfaH
title_full_unstemmed	Origins and Molecular Evolution of the NusG Paralog RfaH
title_sort	origins and molecular evolution of the nusg paralog rfah
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/32768a3b208340efa1e37e8b13041b6b
work_keys_str_mv	AT bingwang originsandmolecularevolutionofthenusgparalogrfah AT vadimmgumerov originsandmolecularevolutionofthenusgparalogrfah AT ekaterinapandrianova originsandmolecularevolutionofthenusgparalogrfah AT igorbzhulin originsandmolecularevolutionofthenusgparalogrfah AT irinaartsimovitch originsandmolecularevolutionofthenusgparalogrfah
_version_	1718426895234629632

Origins and Molecular Evolution of the NusG Paralog RfaH

Ejemplares similares