A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis

Autores
Grau, Roberto Ricardo; de Oña, Paula; Kunert, Maritta; Leñini, Cecilia Andrea; Gallegos Monterrosa, Ramses; Mhatre, Eisha; Vileta, Darío; Donato, Veronica; Hölscher, Theresa; Boland, Wilhem; Kuipers, Oscar P.; Kovács, Ákos T.
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Multicellular biofilm formation and surface motility are bacterial behaviors considered mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi (phosphorylated Spo0A) governs the flagellum-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots, evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization showed that the machineries of sliding and biofilm formation share the same main components (i.e., surfactin, the hydrophobin BslA, exopolysaccharide, and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discovered that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus-far-unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pi reporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in Δspo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviors uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrates the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviors formerly believed to be antagonistic are coordinately activated in benefit of the bacterium and its interaction with the host.
Fil: Grau, Roberto Ricardo. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: de Oña, Paula. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Kunert, Maritta. Instituto Max Planck Institut Fur Chemische Okologie; Alemania
Fil: Leñini, Cecilia Andrea. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Gallegos Monterrosa, Ramses. Universitat Jena; Alemania
Fil: Mhatre, Eisha. Universitat Jena; Alemania
Fil: Vileta, Darío. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Donato, Veronica. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hölscher, Theresa. Universitat Jena; Alemania
Fil: Boland, Wilhem. Instituto Max Planck Institut Fur Chemische Okologie; Alemania
Fil: Kuipers, Oscar P.. University of Groningen; Países Bajos
Fil: Kovács, Ákos T.. Universitat Jena; Alemania
Materia
Signal Transduction-Cell Differentiation
Phosphorelay-Cell Destiny
Potassium channels
Sliding motility Bacillus subtilis
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:11336/13438
Acceder
id CONICETDig_b4202173b043a177f686a0fc6d2ecbf8
oai_identifier_str oai:ri.conicet.gov.ar:11336/13438
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilisGrau, Roberto Ricardode Oña, PaulaKunert, MarittaLeñini, Cecilia AndreaGallegos Monterrosa, RamsesMhatre, EishaVileta, DaríoDonato, VeronicaHölscher, TheresaBoland, WilhemKuipers, Oscar P.Kovács, Ákos T.Signal Transduction-Cell DifferentiationPhosphorelay-Cell DestinyPotassium channelsSliding motility Bacillus subtilishttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Multicellular biofilm formation and surface motility are bacterial behaviors considered mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi (phosphorylated Spo0A) governs the flagellum-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots, evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization showed that the machineries of sliding and biofilm formation share the same main components (i.e., surfactin, the hydrophobin BslA, exopolysaccharide, and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discovered that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus-far-unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pi reporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in Δspo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviors uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrates the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviors formerly believed to be antagonistic are coordinately activated in benefit of the bacterium and its interaction with the host.Fil: Grau, Roberto Ricardo. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: de Oña, Paula. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Kunert, Maritta. Instituto Max Planck Institut Fur Chemische Okologie; AlemaniaFil: Leñini, Cecilia Andrea. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Gallegos Monterrosa, Ramses. Universitat Jena; AlemaniaFil: Mhatre, Eisha. Universitat Jena; AlemaniaFil: Vileta, Darío. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Donato, Veronica. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Hölscher, Theresa. Universitat Jena; AlemaniaFil: Boland, Wilhem. Instituto Max Planck Institut Fur Chemische Okologie; AlemaniaFil: Kuipers, Oscar P.. University of Groningen; Países BajosFil: Kovács, Ákos T.. Universitat Jena; AlemaniaAmerican Society for Microbiology2015-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/13438Grau, Roberto Ricardo; de Oña, Paula; Kunert, Maritta; Leñini, Cecilia Andrea; Gallegos Monterrosa, Ramses; et al.; A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis; American Society for Microbiology; mBio; 6; 4; 7-2015; 1-16; e00581-152150-7511enginfo:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.00581-15info:eu-repo/semantics/altIdentifier/url/http://mbio.asm.org/content/6/4/e00581-15info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-15T14:38:36Zoai:ri.conicet.gov.ar:11336/13438instacron: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:34982025-10-15 14:38:36.589CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
title A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
spellingShingle A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
Grau, Roberto Ricardo
Signal Transduction-Cell Differentiation
Phosphorelay-Cell Destiny
Potassium channels
Sliding motility Bacillus subtilis
title_short A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
title_full A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
title_fullStr A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
title_full_unstemmed A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
title_sort A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis
dc.creator.none.fl_str_mv Grau, Roberto Ricardo
de Oña, Paula
Kunert, Maritta
Leñini, Cecilia Andrea
Gallegos Monterrosa, Ramses
Mhatre, Eisha
Vileta, Darío
Donato, Veronica
Hölscher, Theresa
Boland, Wilhem
Kuipers, Oscar P.
Kovács, Ákos T.
author Grau, Roberto Ricardo
author_facet Grau, Roberto Ricardo
de Oña, Paula
Kunert, Maritta
Leñini, Cecilia Andrea
Gallegos Monterrosa, Ramses
Mhatre, Eisha
Vileta, Darío
Donato, Veronica
Hölscher, Theresa
Boland, Wilhem
Kuipers, Oscar P.
Kovács, Ákos T.
author_role author
author2 de Oña, Paula
Kunert, Maritta
Leñini, Cecilia Andrea
Gallegos Monterrosa, Ramses
Mhatre, Eisha
Vileta, Darío
Donato, Veronica
Hölscher, Theresa
Boland, Wilhem
Kuipers, Oscar P.
Kovács, Ákos T.
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Signal Transduction-Cell Differentiation
Phosphorelay-Cell Destiny
Potassium channels
Sliding motility Bacillus subtilis
topic Signal Transduction-Cell Differentiation
Phosphorelay-Cell Destiny
Potassium channels
Sliding motility Bacillus subtilis
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Multicellular biofilm formation and surface motility are bacterial behaviors considered mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi (phosphorylated Spo0A) governs the flagellum-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots, evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization showed that the machineries of sliding and biofilm formation share the same main components (i.e., surfactin, the hydrophobin BslA, exopolysaccharide, and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discovered that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus-far-unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pi reporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in Δspo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviors uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrates the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviors formerly believed to be antagonistic are coordinately activated in benefit of the bacterium and its interaction with the host.
Fil: Grau, Roberto Ricardo. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: de Oña, Paula. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Kunert, Maritta. Instituto Max Planck Institut Fur Chemische Okologie; Alemania
Fil: Leñini, Cecilia Andrea. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Gallegos Monterrosa, Ramses. Universitat Jena; Alemania
Fil: Mhatre, Eisha. Universitat Jena; Alemania
Fil: Vileta, Darío. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Donato, Veronica. Universidad Nacional de Rosario. Facultad de Cs.bioquimicas y Farmaceuticas. Departamento de Microbiologia; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hölscher, Theresa. Universitat Jena; Alemania
Fil: Boland, Wilhem. Instituto Max Planck Institut Fur Chemische Okologie; Alemania
Fil: Kuipers, Oscar P.. University of Groningen; Países Bajos
Fil: Kovács, Ákos T.. Universitat Jena; Alemania
description Multicellular biofilm formation and surface motility are bacterial behaviors considered mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi (phosphorylated Spo0A) governs the flagellum-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots, evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization showed that the machineries of sliding and biofilm formation share the same main components (i.e., surfactin, the hydrophobin BslA, exopolysaccharide, and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discovered that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus-far-unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pi reporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in Δspo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviors uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrates the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviors formerly believed to be antagonistic are coordinately activated in benefit of the bacterium and its interaction with the host.
publishDate 2015
dc.date.none.fl_str_mv 2015-07
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/11336/13438
Grau, Roberto Ricardo; de Oña, Paula; Kunert, Maritta; Leñini, Cecilia Andrea; Gallegos Monterrosa, Ramses; et al.; A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis; American Society for Microbiology; mBio; 6; 4; 7-2015; 1-16; e00581-15
2150-7511
url http://hdl.handle.net/11336/13438
identifier_str_mv Grau, Roberto Ricardo; de Oña, Paula; Kunert, Maritta; Leñini, Cecilia Andrea; Gallegos Monterrosa, Ramses; et al.; A duo of Potassium-responsive Histidine Kinases govern the multicellular destiny of Bacillus subtilis; American Society for Microbiology; mBio; 6; 4; 7-2015; 1-16; e00581-15
2150-7511
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.00581-15
info:eu-repo/semantics/altIdentifier/url/http://mbio.asm.org/content/6/4/e00581-15
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 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)
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_ 1846082865627922432
score 13.22299

Publicaciones similares