Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida

The Gram-negative bacterium Pseudomonas putida bears a tuft of flagella at a single cell pole. New flagella must be assembled de novo every cell cycle to secure motility of both daughter cells. Here we show that the coordinated action of FimV, FlhF and FleN sets the location, timing and number of fl...

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Detalles Bibliográficos
Autores: Pulido-Sánchez, M., Leal-Morales, Antonio, López-Sánchez, Aroa, Cava, Felipe, Govantes, Fernando
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/397199
Acceso en línea:http://hdl.handle.net/10261/397199
Access Level:acceso abierto
Palabra clave:Flagella
Pseudomonas
Polar landmark proteins
FimV
FlhF
FleN
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spelling Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putidaPulido-Sánchez, M.Leal-Morales, AntonioLópez-Sánchez, AroaCava, FelipeGovantes, FernandoFlagellaPseudomonasPolar landmark proteinsFimVFlhFFleNThe Gram-negative bacterium Pseudomonas putida bears a tuft of flagella at a single cell pole. New flagella must be assembled de novo every cell cycle to secure motility of both daughter cells. Here we show that the coordinated action of FimV, FlhF and FleN sets the location, timing and number of flagella assembled. The polar landmark proteins FimV and FlhF are independently targeted to the nascent new pole during or shortly after cell division, but FimV stabilizes FlhF association with the cell poles. FlhF determines the polar position of the flagella by targeting early flagellar components to the cell pole and preventing their nucleation at non-polar sites. FlhF also promotes efficient flagellar assembly and indirectly stimulates Class III flagellar promoter activation by promoting secretion of the anti-FliA anti-σ factor FlgM. The MinD-like ATPase FleN partitions between the cell poles and the cytoplasm. Cytoplasmic FleN regulates flagellar number by preventing excessive accumulation of FlhF at the cell poles that may otherwise lead to hyperflagellation, likely by antagonizing FleQ-dependent transcriptional activation. FimV is essential to FleN polar location. FimV and FleN temporally regulate the onset of flagellar assembly by preventing premature polar targeting of FlhF and the ensuing premature targeting of additional flagellar components. Our results shed new light on the mechanisms that ensure the timely assembly of the appropriate number of flagella at the correct polar location in polarly flagellated bacteria.This work was supported by grants PGC2018–097151-B-I00, PID2021–126121-NB-I00 and CEX2020–00108-M from the Spanish Ministerio de Ciencia, Innovación y Universidades, by a predoctoral Formación de Profesorado Universitario contract 19/02899 of the Spanish Ministerio de Educación y Formación Profesional, awarded to M P-S, and by an EMBO Scientific Exchange Grant 9458 from the European Molecular Biology Organization, awarded to M P-S to visit FC's laboratory. Funding for open access publishing provided by Universidad Pablo de Olavide/CBUAWith funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2020–00108-M).Peer reviewedElsevierMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)Ministerio de Ciencia e Innovación (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/397199reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-097151-B-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-126121NB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CEX2020–00108-MThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.micres.2024.128033https://doi.org/10.1016/j.micres.2024.128033Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3971992026-05-22T06:33:51Z
dc.title.none.fl_str_mv Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
title Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
spellingShingle Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
Pulido-Sánchez, M.
Flagella
Pseudomonas
Polar landmark proteins
FimV
FlhF
FleN
title_short Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
title_full Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
title_fullStr Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
title_full_unstemmed Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
title_sort Spatial, temporal and numerical regulation of polar flagella assembly in Pseudomonas putida
dc.creator.none.fl_str_mv Pulido-Sánchez, M.
Leal-Morales, Antonio
López-Sánchez, Aroa
Cava, Felipe
Govantes, Fernando
author Pulido-Sánchez, M.
author_facet Pulido-Sánchez, M.
Leal-Morales, Antonio
López-Sánchez, Aroa
Cava, Felipe
Govantes, Fernando
author_role author
author2 Leal-Morales, Antonio
López-Sánchez, Aroa
Cava, Felipe
Govantes, Fernando
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
Ministerio de Ciencia e Innovación (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Flagella
Pseudomonas
Polar landmark proteins
FimV
FlhF
FleN
topic Flagella
Pseudomonas
Polar landmark proteins
FimV
FlhF
FleN
description The Gram-negative bacterium Pseudomonas putida bears a tuft of flagella at a single cell pole. New flagella must be assembled de novo every cell cycle to secure motility of both daughter cells. Here we show that the coordinated action of FimV, FlhF and FleN sets the location, timing and number of flagella assembled. The polar landmark proteins FimV and FlhF are independently targeted to the nascent new pole during or shortly after cell division, but FimV stabilizes FlhF association with the cell poles. FlhF determines the polar position of the flagella by targeting early flagellar components to the cell pole and preventing their nucleation at non-polar sites. FlhF also promotes efficient flagellar assembly and indirectly stimulates Class III flagellar promoter activation by promoting secretion of the anti-FliA anti-σ factor FlgM. The MinD-like ATPase FleN partitions between the cell poles and the cytoplasm. Cytoplasmic FleN regulates flagellar number by preventing excessive accumulation of FlhF at the cell poles that may otherwise lead to hyperflagellation, likely by antagonizing FleQ-dependent transcriptional activation. FimV is essential to FleN polar location. FimV and FleN temporally regulate the onset of flagellar assembly by preventing premature polar targeting of FlhF and the ensuing premature targeting of additional flagellar components. Our results shed new light on the mechanisms that ensure the timely assembly of the appropriate number of flagella at the correct polar location in polarly flagellated bacteria.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/397199
url http://hdl.handle.net/10261/397199
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PGC2018-097151-B-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2021-126121NB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/CEX2020–00108-M
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.1016/j.micres.2024.128033
https://doi.org/10.1016/j.micres.2024.128033
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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