Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae

Autores
Larotonda, Leticia Inés; Mornico, Damien; Khanna, Varun; Bernal Bayard, Joaquín; Ghigo, Jean Marc; Val, Marie Eve; Comerci, Diego José; Mazel, Didier; Soler Bistue, Alfonso J. C.
Año de publicación
2023
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
It is unclear how gene order within the chromosome influences genome evolution. Bacteria cluster transcription and translation genes close to the replication origin (oriC). In Vibrio cholerae, relocation of s10-spc-α locus (S10), the major locus of ribosomal protein genes, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction in growth rate, fitness, and infectivity. To test the long-term impact of this trait, we evolved 12 populations of V. cholerae strains bearing S10 at an oriC-proximal or an oriC-distal location for 1,000 generations. During the first 250 generations, positive selection was the main force driving mutation. After 1,000 generations, we observed more nonadaptative mutations and hypermutator genotypes. Populations fixed inactivating mutations at many genes linked to virulence: flagellum, chemotaxis, biofilm, and quorum sensing. Throughout the experiment, all populations increased their growth rates. However, those bearing S10 close to oriC remained the fittest, indicating that suppressor mutations cannot compensate for the genomic position of the main ribosomal protein locus. Selection and sequencing of the fastest-growing clones allowed us to characterize mutations inactivating, among other sites, flagellum master regulators. Reintroduction of these mutations into the wild-type context led to a ≈ 10% growth improvement. In conclusion, the genomic location of ribosomal protein genes conditions the evolutionary trajectory of V. cholerae. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and evolution. A lack of suppression enables artificial gene relocation as a tool for genetic circuit reprogramming. IMPORTANCE The bacterial chromosome harbors several entangled processes such as replication, transcription, DNA repair, and segregation. Replication begins bidirectionally at the replication origin (oriC) until the terminal region (ter) organizing the genome along the ori-ter axis gene order along this axis could link genome structure to cell physiology. Fast-growing bacteria cluster translation genes near oriC. In Vibrio cholerae, moving them away was feasible but at the cost of losing fitness and infectivity. Here, we evolved strains harboring ribosomal genes close or far from oriC. Growth rate differences persisted after 1,000 generations. No mutation was able to compensate for the growth defect, showing that ribosomal gene location conditions their evolutionary trajectory. Despite the high plasticity of bacterial genomes, evolution has sculpted gene order to optimize the ecological strategy of the microorganism. We observed growth rate improvement throughout the evolution experiment that occurred at expense of energetically costly processes such the flagellum biosynthesis and virulence-related functions. From the biotechnological point of view, manipulation of gene order enables altering bacterial growth with no escape events.
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: Mornico, Damien. Centre National de la Recherche Scientifique; Francia
Fil: Khanna, Varun. Centre National de la Recherche Scientifique; Francia
Fil: Bernal Bayard, Joaquín. Universidad de Sevilla; España
Fil: Ghigo, Jean Marc. Centre National de la Recherche Scientifique; Francia
Fil: Val, Marie Eve. Centre National de la Recherche Scientifique; Francia
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: Mazel, Didier. Centre National de la Recherche Scientifique; 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
EXPERIMENTAL EVOLUTION
GENOMICS
GROWTH RATE
RIBOSOMAL PROTEIN
VIBRIO CHOLERAE
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:11336/228799

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oai_identifier_str oai:ri.conicet.gov.ar:11336/228799
network_acronym_str CONICETDig
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network_name_str CONICET Digital (CONICET)
spelling Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio choleraeLarotonda, Leticia InésMornico, DamienKhanna, VarunBernal Bayard, JoaquínGhigo, Jean MarcVal, Marie EveComerci, Diego JoséMazel, DidierSoler Bistue, Alfonso J. C.EXPERIMENTAL EVOLUTIONGENOMICSGROWTH RATERIBOSOMAL PROTEINVIBRIO CHOLERAEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1It is unclear how gene order within the chromosome influences genome evolution. Bacteria cluster transcription and translation genes close to the replication origin (oriC). In Vibrio cholerae, relocation of s10-spc-α locus (S10), the major locus of ribosomal protein genes, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction in growth rate, fitness, and infectivity. To test the long-term impact of this trait, we evolved 12 populations of V. cholerae strains bearing S10 at an oriC-proximal or an oriC-distal location for 1,000 generations. During the first 250 generations, positive selection was the main force driving mutation. After 1,000 generations, we observed more nonadaptative mutations and hypermutator genotypes. Populations fixed inactivating mutations at many genes linked to virulence: flagellum, chemotaxis, biofilm, and quorum sensing. Throughout the experiment, all populations increased their growth rates. However, those bearing S10 close to oriC remained the fittest, indicating that suppressor mutations cannot compensate for the genomic position of the main ribosomal protein locus. Selection and sequencing of the fastest-growing clones allowed us to characterize mutations inactivating, among other sites, flagellum master regulators. Reintroduction of these mutations into the wild-type context led to a ≈ 10% growth improvement. In conclusion, the genomic location of ribosomal protein genes conditions the evolutionary trajectory of V. cholerae. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and evolution. A lack of suppression enables artificial gene relocation as a tool for genetic circuit reprogramming. IMPORTANCE The bacterial chromosome harbors several entangled processes such as replication, transcription, DNA repair, and segregation. Replication begins bidirectionally at the replication origin (oriC) until the terminal region (ter) organizing the genome along the ori-ter axis gene order along this axis could link genome structure to cell physiology. Fast-growing bacteria cluster translation genes near oriC. In Vibrio cholerae, moving them away was feasible but at the cost of losing fitness and infectivity. Here, we evolved strains harboring ribosomal genes close or far from oriC. Growth rate differences persisted after 1,000 generations. No mutation was able to compensate for the growth defect, showing that ribosomal gene location conditions their evolutionary trajectory. Despite the high plasticity of bacterial genomes, evolution has sculpted gene order to optimize the ecological strategy of the microorganism. We observed growth rate improvement throughout the evolution experiment that occurred at expense of energetically costly processes such the flagellum biosynthesis and virulence-related functions. From the biotechnological point of view, manipulation of gene order enables altering bacterial growth with no escape events.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: Mornico, Damien. Centre National de la Recherche Scientifique; FranciaFil: Khanna, Varun. Centre National de la Recherche Scientifique; FranciaFil: Bernal Bayard, Joaquín. Universidad de Sevilla; EspañaFil: Ghigo, Jean Marc. Centre National de la Recherche Scientifique; FranciaFil: Val, Marie Eve. Centre National de la Recherche Scientifique; FranciaFil: 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: Mazel, Didier. Centre National de la Recherche Scientifique; 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; ArgentinaAmerican Society for Microbiology2023-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/228799Larotonda, Leticia Inés; Mornico, Damien; Khanna, Varun; Bernal Bayard, Joaquín; Ghigo, Jean Marc; et al.; Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae; American Society for Microbiology; mBio; 14; 2; 3-2023; 1-192150-7511CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.asm.org/doi/10.1128/mbio.03432-22info:eu-repo/semantics/altIdentifier/doi/10.1128/mbio.03432-22info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:36:25Zoai:ri.conicet.gov.ar:11336/228799instacron: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:34982025-09-29 10:36:25.694CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
title Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
spellingShingle Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
Larotonda, Leticia Inés
EXPERIMENTAL EVOLUTION
GENOMICS
GROWTH RATE
RIBOSOMAL PROTEIN
VIBRIO CHOLERAE
title_short Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
title_full Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
title_fullStr Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
title_full_unstemmed Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
title_sort Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae
dc.creator.none.fl_str_mv Larotonda, Leticia Inés
Mornico, Damien
Khanna, Varun
Bernal Bayard, Joaquín
Ghigo, Jean Marc
Val, Marie Eve
Comerci, Diego José
Mazel, Didier
Soler Bistue, Alfonso J. C.
author Larotonda, Leticia Inés
author_facet Larotonda, Leticia Inés
Mornico, Damien
Khanna, Varun
Bernal Bayard, Joaquín
Ghigo, Jean Marc
Val, Marie Eve
Comerci, Diego José
Mazel, Didier
Soler Bistue, Alfonso J. C.
author_role author
author2 Mornico, Damien
Khanna, Varun
Bernal Bayard, Joaquín
Ghigo, Jean Marc
Val, Marie Eve
Comerci, Diego José
Mazel, Didier
Soler Bistue, Alfonso J. C.
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv EXPERIMENTAL EVOLUTION
GENOMICS
GROWTH RATE
RIBOSOMAL PROTEIN
VIBRIO CHOLERAE
topic EXPERIMENTAL EVOLUTION
GENOMICS
GROWTH RATE
RIBOSOMAL PROTEIN
VIBRIO CHOLERAE
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv It is unclear how gene order within the chromosome influences genome evolution. Bacteria cluster transcription and translation genes close to the replication origin (oriC). In Vibrio cholerae, relocation of s10-spc-α locus (S10), the major locus of ribosomal protein genes, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction in growth rate, fitness, and infectivity. To test the long-term impact of this trait, we evolved 12 populations of V. cholerae strains bearing S10 at an oriC-proximal or an oriC-distal location for 1,000 generations. During the first 250 generations, positive selection was the main force driving mutation. After 1,000 generations, we observed more nonadaptative mutations and hypermutator genotypes. Populations fixed inactivating mutations at many genes linked to virulence: flagellum, chemotaxis, biofilm, and quorum sensing. Throughout the experiment, all populations increased their growth rates. However, those bearing S10 close to oriC remained the fittest, indicating that suppressor mutations cannot compensate for the genomic position of the main ribosomal protein locus. Selection and sequencing of the fastest-growing clones allowed us to characterize mutations inactivating, among other sites, flagellum master regulators. Reintroduction of these mutations into the wild-type context led to a ≈ 10% growth improvement. In conclusion, the genomic location of ribosomal protein genes conditions the evolutionary trajectory of V. cholerae. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and evolution. A lack of suppression enables artificial gene relocation as a tool for genetic circuit reprogramming. IMPORTANCE The bacterial chromosome harbors several entangled processes such as replication, transcription, DNA repair, and segregation. Replication begins bidirectionally at the replication origin (oriC) until the terminal region (ter) organizing the genome along the ori-ter axis gene order along this axis could link genome structure to cell physiology. Fast-growing bacteria cluster translation genes near oriC. In Vibrio cholerae, moving them away was feasible but at the cost of losing fitness and infectivity. Here, we evolved strains harboring ribosomal genes close or far from oriC. Growth rate differences persisted after 1,000 generations. No mutation was able to compensate for the growth defect, showing that ribosomal gene location conditions their evolutionary trajectory. Despite the high plasticity of bacterial genomes, evolution has sculpted gene order to optimize the ecological strategy of the microorganism. We observed growth rate improvement throughout the evolution experiment that occurred at expense of energetically costly processes such the flagellum biosynthesis and virulence-related functions. From the biotechnological point of view, manipulation of gene order enables altering bacterial growth with no escape events.
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: Mornico, Damien. Centre National de la Recherche Scientifique; Francia
Fil: Khanna, Varun. Centre National de la Recherche Scientifique; Francia
Fil: Bernal Bayard, Joaquín. Universidad de Sevilla; España
Fil: Ghigo, Jean Marc. Centre National de la Recherche Scientifique; Francia
Fil: Val, Marie Eve. Centre National de la Recherche Scientifique; Francia
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: Mazel, Didier. Centre National de la Recherche Scientifique; 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 It is unclear how gene order within the chromosome influences genome evolution. Bacteria cluster transcription and translation genes close to the replication origin (oriC). In Vibrio cholerae, relocation of s10-spc-α locus (S10), the major locus of ribosomal protein genes, to ectopic genomic positions shows that its relative distance to the oriC correlates to a reduction in growth rate, fitness, and infectivity. To test the long-term impact of this trait, we evolved 12 populations of V. cholerae strains bearing S10 at an oriC-proximal or an oriC-distal location for 1,000 generations. During the first 250 generations, positive selection was the main force driving mutation. After 1,000 generations, we observed more nonadaptative mutations and hypermutator genotypes. Populations fixed inactivating mutations at many genes linked to virulence: flagellum, chemotaxis, biofilm, and quorum sensing. Throughout the experiment, all populations increased their growth rates. However, those bearing S10 close to oriC remained the fittest, indicating that suppressor mutations cannot compensate for the genomic position of the main ribosomal protein locus. Selection and sequencing of the fastest-growing clones allowed us to characterize mutations inactivating, among other sites, flagellum master regulators. Reintroduction of these mutations into the wild-type context led to a ≈ 10% growth improvement. In conclusion, the genomic location of ribosomal protein genes conditions the evolutionary trajectory of V. cholerae. While genomic content is highly plastic in prokaryotes, gene order is an underestimated factor that conditions cellular physiology and evolution. A lack of suppression enables artificial gene relocation as a tool for genetic circuit reprogramming. IMPORTANCE The bacterial chromosome harbors several entangled processes such as replication, transcription, DNA repair, and segregation. Replication begins bidirectionally at the replication origin (oriC) until the terminal region (ter) organizing the genome along the ori-ter axis gene order along this axis could link genome structure to cell physiology. Fast-growing bacteria cluster translation genes near oriC. In Vibrio cholerae, moving them away was feasible but at the cost of losing fitness and infectivity. Here, we evolved strains harboring ribosomal genes close or far from oriC. Growth rate differences persisted after 1,000 generations. No mutation was able to compensate for the growth defect, showing that ribosomal gene location conditions their evolutionary trajectory. Despite the high plasticity of bacterial genomes, evolution has sculpted gene order to optimize the ecological strategy of the microorganism. We observed growth rate improvement throughout the evolution experiment that occurred at expense of energetically costly processes such the flagellum biosynthesis and virulence-related functions. From the biotechnological point of view, manipulation of gene order enables altering bacterial growth with no escape events.
publishDate 2023
dc.date.none.fl_str_mv 2023-03
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/11336/228799
Larotonda, Leticia Inés; Mornico, Damien; Khanna, Varun; Bernal Bayard, Joaquín; Ghigo, Jean Marc; et al.; Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae; American Society for Microbiology; mBio; 14; 2; 3-2023; 1-19
2150-7511
CONICET Digital
CONICET
url http://hdl.handle.net/11336/228799
identifier_str_mv Larotonda, Leticia Inés; Mornico, Damien; Khanna, Varun; Bernal Bayard, Joaquín; Ghigo, Jean Marc; et al.; Chromosomal Position of Ribosomal Protein Genes Affects Long-Term Evolution of Vibrio cholerae; American Society for Microbiology; mBio; 14; 2; 3-2023; 1-19
2150-7511
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://journals.asm.org/doi/10.1128/mbio.03432-22
info:eu-repo/semantics/altIdentifier/doi/10.1128/mbio.03432-22
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
application/pdf
dc.publisher.none.fl_str_mv American Society for Microbiology
publisher.none.fl_str_mv American Society for Microbiology
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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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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