Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria

Autores
Larotonda, Leticia Inés; Ojeda, Elisa; Guzzi, Noa; Bordignon, María Belén; Fulgenzi, Fabiana Rosa; Comerci, Diego José; Llorente, Briardo; Mazel, Didier; Loot, Céline; Val, Marie-Eve; Soler Bistue, Alfonso J. C.
Año de publicación
2026
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
How gene order along chromosomes affects cellular homeostasis and genome evolution remains poorly understood. Bacterial chromosomes are organized along the replication origin (oriC)-terminus (ter) axis. The spatial arrangement of genes within this axis may influence cellular physiology, genome evolution, and transcriptional regulation. We tested the importance of the universally conserved rplKAJL-rpoBC locus, which encodes the β/β´ subunits of the sole bacterial RNA polymerase (RNAP), by relocating it to different genomic positions in the fast-growing pathogen Vibrio cholerae. Relocation close from locus native site was neutral but relocating it near either chromosomal terminus reduced exponential growth and competitive fitness specifically in nutrient-rich media. Marker-frequency analysis showed that distal positioning lowered locus copy number from ~3 to ~1 per cell, causing a 20%-25% depletion in cellular RNAP without altering its subcellular distribution. Introducing an additional oriC-proximal copy restored wild-type phenotypes, whereas two terminus copies rescued growth solely through increased dosage. Deleting the oriC-proximal RNAP genes reproduced all defects, identifying them as the primary drivers. Selection keeps RNAP genes close to oriC to harness replication-associated dosage increment during exponential growth, ensuring adequate transcription capacity for rapid proliferation. Gene order is a key but overlooked layer of bacterial genome evolution and ecological adaptation.
Fil: Larotonda, Leticia Inés. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Ojeda, Elisa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Guzzi, Noa. Institut Pasteur de Paris.; Francia
Fil: Bordignon, María Belén. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Fulgenzi, Fabiana Rosa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Comerci, Diego José. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Llorente, Briardo. Macquarie University. Faculty Of Science And Engineering. Department Of Molecular Sciences.; Australia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Mazel, Didier. Institut Pasteur de Paris.; Francia
Fil: Loot, Céline. Institut Pasteur de Paris.; Francia
Fil: Val, Marie-Eve. Institut Pasteur de Paris.; Francia
Fil: Soler Bistue, Alfonso J. C.. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Materia
RNA polymerase
chromosome
Vibrio cholerae
growth rate
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/290129
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/290129
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteriaLarotonda, Leticia InésOjeda, ElisaGuzzi, NoaBordignon, María BelénFulgenzi, Fabiana RosaComerci, Diego JoséLlorente, BriardoMazel, DidierLoot, CélineVal, Marie-EveSoler Bistue, Alfonso J. C.RNA polymerasechromosomeVibrio choleraegrowth ratehttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1How gene order along chromosomes affects cellular homeostasis and genome evolution remains poorly understood. Bacterial chromosomes are organized along the replication origin (oriC)-terminus (ter) axis. The spatial arrangement of genes within this axis may influence cellular physiology, genome evolution, and transcriptional regulation. We tested the importance of the universally conserved rplKAJL-rpoBC locus, which encodes the β/β´ subunits of the sole bacterial RNA polymerase (RNAP), by relocating it to different genomic positions in the fast-growing pathogen Vibrio cholerae. Relocation close from locus native site was neutral but relocating it near either chromosomal terminus reduced exponential growth and competitive fitness specifically in nutrient-rich media. Marker-frequency analysis showed that distal positioning lowered locus copy number from ~3 to ~1 per cell, causing a 20%-25% depletion in cellular RNAP without altering its subcellular distribution. Introducing an additional oriC-proximal copy restored wild-type phenotypes, whereas two terminus copies rescued growth solely through increased dosage. Deleting the oriC-proximal RNAP genes reproduced all defects, identifying them as the primary drivers. Selection keeps RNAP genes close to oriC to harness replication-associated dosage increment during exponential growth, ensuring adequate transcription capacity for rapid proliferation. Gene order is a key but overlooked layer of bacterial genome evolution and ecological adaptation.Fil: Larotonda, Leticia Inés. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Ojeda, Elisa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Guzzi, Noa. Institut Pasteur de Paris.; FranciaFil: Bordignon, María Belén. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Fulgenzi, Fabiana Rosa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Comerci, Diego José. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Llorente, Briardo. Macquarie University. Faculty Of Science And Engineering. Department Of Molecular Sciences.; Australia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Mazel, Didier. Institut Pasteur de Paris.; FranciaFil: Loot, Céline. Institut Pasteur de Paris.; FranciaFil: Val, Marie-Eve. Institut Pasteur de Paris.; FranciaFil: Soler Bistue, Alfonso J. C.. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; ArgentinaOxford University Press2026-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/290129Larotonda, Leticia Inés; Ojeda, Elisa; Guzzi, Noa; Bordignon, María Belén; Fulgenzi, Fabiana Rosa; et al.; Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria; Oxford University Press; Nucleic Acids Research; 54; 5; 3-2026; 1-170305-10481362-4962CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article/doi/10.1093/nar/gkag222/8526023info:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gkag222info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2026-08-25T15:49:51Zoai:ri.conicet.gov.ar:11336/290129instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982026-08-25 15:49:51.544CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
title Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
spellingShingle Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
Larotonda, Leticia Inés
RNA polymerase
chromosome
Vibrio cholerae
growth rate
title_short Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
title_full Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
title_fullStr Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
title_full_unstemmed Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
title_sort Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria
dc.creator.none.fl_str_mv Larotonda, Leticia Inés
Ojeda, Elisa
Guzzi, Noa
Bordignon, María Belén
Fulgenzi, Fabiana Rosa
Comerci, Diego José
Llorente, Briardo
Mazel, Didier
Loot, Céline
Val, Marie-Eve
Soler Bistue, Alfonso J. C.
author Larotonda, Leticia Inés
author_facet Larotonda, Leticia Inés
Ojeda, Elisa
Guzzi, Noa
Bordignon, María Belén
Fulgenzi, Fabiana Rosa
Comerci, Diego José
Llorente, Briardo
Mazel, Didier
Loot, Céline
Val, Marie-Eve
Soler Bistue, Alfonso J. C.
author_role author
author2 Ojeda, Elisa
Guzzi, Noa
Bordignon, María Belén
Fulgenzi, Fabiana Rosa
Comerci, Diego José
Llorente, Briardo
Mazel, Didier
Loot, Céline
Val, Marie-Eve
Soler Bistue, Alfonso J. C.
author2_role author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv RNA polymerase
chromosome
Vibrio cholerae
growth rate
topic RNA polymerase
chromosome
Vibrio cholerae
growth rate
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv How gene order along chromosomes affects cellular homeostasis and genome evolution remains poorly understood. Bacterial chromosomes are organized along the replication origin (oriC)-terminus (ter) axis. The spatial arrangement of genes within this axis may influence cellular physiology, genome evolution, and transcriptional regulation. We tested the importance of the universally conserved rplKAJL-rpoBC locus, which encodes the β/β´ subunits of the sole bacterial RNA polymerase (RNAP), by relocating it to different genomic positions in the fast-growing pathogen Vibrio cholerae. Relocation close from locus native site was neutral but relocating it near either chromosomal terminus reduced exponential growth and competitive fitness specifically in nutrient-rich media. Marker-frequency analysis showed that distal positioning lowered locus copy number from ~3 to ~1 per cell, causing a 20%-25% depletion in cellular RNAP without altering its subcellular distribution. Introducing an additional oriC-proximal copy restored wild-type phenotypes, whereas two terminus copies rescued growth solely through increased dosage. Deleting the oriC-proximal RNAP genes reproduced all defects, identifying them as the primary drivers. Selection keeps RNAP genes close to oriC to harness replication-associated dosage increment during exponential growth, ensuring adequate transcription capacity for rapid proliferation. Gene order is a key but overlooked layer of bacterial genome evolution and ecological adaptation.
Fil: Larotonda, Leticia Inés. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Ojeda, Elisa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Guzzi, Noa. Institut Pasteur de Paris.; Francia
Fil: Bordignon, María Belén. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Fulgenzi, Fabiana Rosa. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Comerci, Diego José. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Llorente, Briardo. Macquarie University. Faculty Of Science And Engineering. Department Of Molecular Sciences.; Australia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Mazel, Didier. Institut Pasteur de Paris.; Francia
Fil: Loot, Céline. Institut Pasteur de Paris.; Francia
Fil: Val, Marie-Eve. Institut Pasteur de Paris.; Francia
Fil: Soler Bistue, Alfonso J. C.. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas. - Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Biotecnológicas; Argentina
description How gene order along chromosomes affects cellular homeostasis and genome evolution remains poorly understood. Bacterial chromosomes are organized along the replication origin (oriC)-terminus (ter) axis. The spatial arrangement of genes within this axis may influence cellular physiology, genome evolution, and transcriptional regulation. We tested the importance of the universally conserved rplKAJL-rpoBC locus, which encodes the β/β´ subunits of the sole bacterial RNA polymerase (RNAP), by relocating it to different genomic positions in the fast-growing pathogen Vibrio cholerae. Relocation close from locus native site was neutral but relocating it near either chromosomal terminus reduced exponential growth and competitive fitness specifically in nutrient-rich media. Marker-frequency analysis showed that distal positioning lowered locus copy number from ~3 to ~1 per cell, causing a 20%-25% depletion in cellular RNAP without altering its subcellular distribution. Introducing an additional oriC-proximal copy restored wild-type phenotypes, whereas two terminus copies rescued growth solely through increased dosage. Deleting the oriC-proximal RNAP genes reproduced all defects, identifying them as the primary drivers. Selection keeps RNAP genes close to oriC to harness replication-associated dosage increment during exponential growth, ensuring adequate transcription capacity for rapid proliferation. Gene order is a key but overlooked layer of bacterial genome evolution and ecological adaptation.
publishDate 2026
dc.date.none.fl_str_mv 2026-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/290129
Larotonda, Leticia Inés; Ojeda, Elisa; Guzzi, Noa; Bordignon, María Belén; Fulgenzi, Fabiana Rosa; et al.; Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria; Oxford University Press; Nucleic Acids Research; 54; 5; 3-2026; 1-17
0305-1048
1362-4962
CONICET Digital
CONICET
url http://hdl.handle.net/11336/290129
identifier_str_mv Larotonda, Leticia Inés; Ojeda, Elisa; Guzzi, Noa; Bordignon, María Belén; Fulgenzi, Fabiana Rosa; et al.; Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria; Oxford University Press; Nucleic Acids Research; 54; 5; 3-2026; 1-17
0305-1048
1362-4962
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://academic.oup.com/nar/article/doi/10.1093/nar/gkag222/8526023
info:eu-repo/semantics/altIdentifier/doi/10.1093/nar/gkag222
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.265058

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