Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae

Autores
Soler Bistue, Alfonso J. C.; Aguilar Pierlé, Sebastián; Garcia Garcerá, Marc; Val, Marie Eve; Sismeiro, Odile; Varet, Hugo; Sieira, Rodrigo; Krin, Evelyne; Skovgaard, Ole; Comerci, Diego José; Rocha, Eduardo P. C.; Mazel, Didier
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined.We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains.The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth.
Fil: Soler Bistue, Alfonso J. C.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Aguilar Pierlé, Sebastián. Institut Pasteur; Francia
Fil: Garcia Garcerá, Marc. Institut Pasteur; Francia
Fil: Val, Marie Eve. Institut Pasteur; Francia
Fil: Sismeiro, Odile. Institut Pasteur; Francia
Fil: Varet, Hugo. Institut Pasteur; Francia
Fil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Krin, Evelyne. Institut Pasteur; Francia
Fil: Skovgaard, Ole. Roskilde Universitet; Dinamarca
Fil: Comerci, Diego José. Universidad Nacional de San Martin. Instituto de Investigaciones Biotecnologicas. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Oficina de Coordinacion Administrativa Pque. Centenario. Instituto de Investigaciones Biotecnologicas.; Argentina
Fil: Rocha, Eduardo P. C.. Institut Pasteur; Francia
Fil: Mazel, Didier. Institut Pasteur; Francia
Materia
VIBRIO CHOLERAE
RIBOSOMAL PROTEINS
GROWTH RATE
GENOMICS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/112160
Acceder
id CONICETDig_cbc1553f952baffb70819b953eb1671e
oai_identifier_str oai:ri.conicet.gov.ar:11336/112160
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio choleraeSoler Bistue, Alfonso J. C.Aguilar Pierlé, SebastiánGarcia Garcerá, MarcVal, Marie EveSismeiro, OdileVaret, HugoSieira, RodrigoKrin, EvelyneSkovgaard, OleComerci, Diego JoséRocha, Eduardo P. C.Mazel, DidierVIBRIO CHOLERAERIBOSOMAL PROTEINSGROWTH RATEGENOMICShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined.We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains.The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth.Fil: Soler Bistue, Alfonso J. C.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; ArgentinaFil: Aguilar Pierlé, Sebastián. Institut Pasteur; FranciaFil: Garcia Garcerá, Marc. Institut Pasteur; FranciaFil: Val, Marie Eve. Institut Pasteur; FranciaFil: Sismeiro, Odile. Institut Pasteur; FranciaFil: Varet, Hugo. Institut Pasteur; FranciaFil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; ArgentinaFil: Krin, Evelyne. Institut Pasteur; FranciaFil: Skovgaard, Ole. Roskilde Universitet; DinamarcaFil: Comerci, Diego José. Universidad Nacional de San Martin. Instituto de Investigaciones Biotecnologicas. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Oficina de Coordinacion Administrativa Pque. Centenario. Instituto de Investigaciones Biotecnologicas.; ArgentinaFil: Rocha, Eduardo P. C.. Institut Pasteur; FranciaFil: Mazel, Didier. Institut Pasteur; FranciaBioMed Central2020-04info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/112160Soler Bistue, Alfonso J. C.; Aguilar Pierlé, Sebastián; Garcia Garcerá, Marc; Val, Marie Eve; Sismeiro, Odile; et al.; Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae; BioMed Central; Bmc Biology; 18; 1; 4-2020; 1-181741-7007CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-020-00777-5info:eu-repo/semantics/altIdentifier/doi/10.1186/s12915-020-00777-5info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:12:13Zoai:ri.conicet.gov.ar:11336/112160instacron: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:34982025-10-22 11:12:13.566CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
title Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
spellingShingle Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
Soler Bistue, Alfonso J. C.
VIBRIO CHOLERAE
RIBOSOMAL PROTEINS
GROWTH RATE
GENOMICS
title_short Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
title_full Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
title_fullStr Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
title_full_unstemmed Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
title_sort Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae
dc.creator.none.fl_str_mv Soler Bistue, Alfonso J. C.
Aguilar Pierlé, Sebastián
Garcia Garcerá, Marc
Val, Marie Eve
Sismeiro, Odile
Varet, Hugo
Sieira, Rodrigo
Krin, Evelyne
Skovgaard, Ole
Comerci, Diego José
Rocha, Eduardo P. C.
Mazel, Didier
author Soler Bistue, Alfonso J. C.
author_facet Soler Bistue, Alfonso J. C.
Aguilar Pierlé, Sebastián
Garcia Garcerá, Marc
Val, Marie Eve
Sismeiro, Odile
Varet, Hugo
Sieira, Rodrigo
Krin, Evelyne
Skovgaard, Ole
Comerci, Diego José
Rocha, Eduardo P. C.
Mazel, Didier
author_role author
author2 Aguilar Pierlé, Sebastián
Garcia Garcerá, Marc
Val, Marie Eve
Sismeiro, Odile
Varet, Hugo
Sieira, Rodrigo
Krin, Evelyne
Skovgaard, Ole
Comerci, Diego José
Rocha, Eduardo P. C.
Mazel, Didier
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv VIBRIO CHOLERAE
RIBOSOMAL PROTEINS
GROWTH RATE
GENOMICS
topic VIBRIO CHOLERAE
RIBOSOMAL PROTEINS
GROWTH RATE
GENOMICS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined.We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains.The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth.
Fil: Soler Bistue, Alfonso J. C.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Investigaciones Biotecnológicas. Universidad Nacional de San Martín. Instituto de Investigaciones Biotecnológicas; Argentina
Fil: Aguilar Pierlé, Sebastián. Institut Pasteur; Francia
Fil: Garcia Garcerá, Marc. Institut Pasteur; Francia
Fil: Val, Marie Eve. Institut Pasteur; Francia
Fil: Sismeiro, Odile. Institut Pasteur; Francia
Fil: Varet, Hugo. Institut Pasteur; Francia
Fil: Sieira, Rodrigo. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Bioquímicas de Buenos Aires. Fundación Instituto Leloir. Instituto de Investigaciones Bioquímicas de Buenos Aires; Argentina
Fil: Krin, Evelyne. Institut Pasteur; Francia
Fil: Skovgaard, Ole. Roskilde Universitet; Dinamarca
Fil: Comerci, Diego José. Universidad Nacional de San Martin. Instituto de Investigaciones Biotecnologicas. - Consejo Nacional de Investigaciones Cientificas y Tecnicas. Oficina de Coordinacion Administrativa Pque. Centenario. Instituto de Investigaciones Biotecnologicas.; Argentina
Fil: Rocha, Eduardo P. C.. Institut Pasteur; Francia
Fil: Mazel, Didier. Institut Pasteur; Francia
description In fast-growing bacteria, the genomic location of ribosomal protein (RP) genes is biased towards the replication origin (oriC). This trait allows optimizing their expression during exponential phase since oriC neighboring regions are in higher dose due to multifork replication. Relocation of s10-spc-α locus (S10), which codes for most of the RP, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction on its dosage, its expression, and bacterial growth rate. However, a mechanism linking S10 dosage to cell physiology has still not been determined.We hypothesized that S10 dosage perturbations impact protein synthesis capacity. Strikingly, we observed that in Vibrio cholerae, protein production capacity was independent of S10 position. Deep sequencing revealed that S10 relocation altered chromosomal replication dynamics and genome-wide transcription. Such changes increased as a function of oriC-S10 distance. Since RP constitutes a large proportion of cell mass, lower S10 dosage could lead to changes in macromolecular crowding, impacting cell physiology. Accordingly, cytoplasm fluidity was higher in mutants where S10 is most distant from oriC. In hyperosmotic conditions, when crowding differences are minimized, the growth rate and replication dynamics were highly alleviated in these strains.The genomic location of RP genes ensures its optimal dosage. However, besides of its essential function in translation, their genomic position sustains an optimal macromolecular crowding essential for maximizing growth. Hence, this could be another mechanism coordinating DNA replication to bacterial growth.
publishDate 2020
dc.date.none.fl_str_mv 2020-04
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/11336/112160
Soler Bistue, Alfonso J. C.; Aguilar Pierlé, Sebastián; Garcia Garcerá, Marc; Val, Marie Eve; Sismeiro, Odile; et al.; Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae; BioMed Central; Bmc Biology; 18; 1; 4-2020; 1-18
1741-7007
CONICET Digital
CONICET
url http://hdl.handle.net/11336/112160
identifier_str_mv Soler Bistue, Alfonso J. C.; Aguilar Pierlé, Sebastián; Garcia Garcerá, Marc; Val, Marie Eve; Sismeiro, Odile; et al.; Macromolecular crowding links ribosomal protein gene dosage to growth rate in Vibrio cholerae; BioMed Central; Bmc Biology; 18; 1; 4-2020; 1-18
1741-7007
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://bmcbiol.biomedcentral.com/articles/10.1186/s12915-020-00777-5
info:eu-repo/semantics/altIdentifier/doi/10.1186/s12915-020-00777-5
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
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
_version_ 1846781512012267520
score 12.982451

Publicaciones similares