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
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/228799
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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) |
collection |
CONICET Digital (CONICET) |
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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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13.070432 |