The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives

Autores
Ramos Ricciutti, Fernando; Soldano, Anabel; Herrera Seitz, Karina; Gasperotti, Ana Florencia; Boyko, Alexandra; Jung, Kirsten; Bellinzoni, Marco; Lisa, María Natalia; Studdert, Claudia Alicia
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The chemosensory pathway HtChe2 from the marine bacterium Halomonas titanicae KHS3 controls the activity of a diguanylate cyclase. Constitutive activation of this pathway results in colony morphology alterations and an increased ability to form biofilm. Such characteristics resemble the behavior of the Wsp pathway of Pseudomonas. In this work, we investigate the specificity of Htc10, the only chemoreceptor coded within the HtChe2 gene cluster. The purine derivatives guanine and hypoxanthine were identified as ligands of the recombinantly produced Htc10 ligand-binding domain, with dissociation constants in the micromolar range, and its structure was solved by X-ray protein crystallography. The sensor domain of Htc10 adopts a double Cache folding, with ligands bound to the membrane-distal pocket. A high-resolution structure of the occupied guanine-binding pocket allowed the identification of residues involved in ligand recognition. Such residues were validated by site-directed mutagenesis and isothermal titration calorimetry analyses of the protein variants. Moreover, heterologous expression of Htc10 in a Pseudomonas putida mutant lacking the native Wsp chemoreceptor promoted biofilm formation, a phenotype that was further enhanced by Htc10-specific ligands. To our knowledge, this is the first description of binding specificity of a chemoreceptor that controls the activity of an associated diguanylate cyclase, opening the way for dynamic studies of the signaling behavior of this kind of sensory complex.
Fil: Ramos Ricciutti, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Soldano, Anabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Herrera Seitz, Karina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Gasperotti, Ana Florencia. Ludwig Maximilians Universitat; Alemania
Fil: Boyko, Alexandra. Instituto Pasteur; Francia
Fil: Jung, Kirsten. Ludwig Maximilians Universitat; Alemania
Fil: Bellinzoni, Marco. Instituto Pasteur; Francia
Fil: Lisa, María Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. Plataforma de Biología Estructural y Metabolómica; Argentina
Fil: Studdert, Claudia Alicia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Materia
HALOMONAS
CHEMORECEPTORS
GUANINE-BINDING
DOUBLE-CACHE SENSOR DOMAIN
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/265492
Acceder
id CONICETDig_6eed5cd39907911617a136310d37fd32
oai_identifier_str oai:ri.conicet.gov.ar:11336/265492
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivativesRamos Ricciutti, FernandoSoldano, AnabelHerrera Seitz, KarinaGasperotti, Ana FlorenciaBoyko, AlexandraJung, KirstenBellinzoni, MarcoLisa, María NataliaStuddert, Claudia AliciaHALOMONASCHEMORECEPTORSGUANINE-BINDINGDOUBLE-CACHE SENSOR DOMAINhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The chemosensory pathway HtChe2 from the marine bacterium Halomonas titanicae KHS3 controls the activity of a diguanylate cyclase. Constitutive activation of this pathway results in colony morphology alterations and an increased ability to form biofilm. Such characteristics resemble the behavior of the Wsp pathway of Pseudomonas. In this work, we investigate the specificity of Htc10, the only chemoreceptor coded within the HtChe2 gene cluster. The purine derivatives guanine and hypoxanthine were identified as ligands of the recombinantly produced Htc10 ligand-binding domain, with dissociation constants in the micromolar range, and its structure was solved by X-ray protein crystallography. The sensor domain of Htc10 adopts a double Cache folding, with ligands bound to the membrane-distal pocket. A high-resolution structure of the occupied guanine-binding pocket allowed the identification of residues involved in ligand recognition. Such residues were validated by site-directed mutagenesis and isothermal titration calorimetry analyses of the protein variants. Moreover, heterologous expression of Htc10 in a Pseudomonas putida mutant lacking the native Wsp chemoreceptor promoted biofilm formation, a phenotype that was further enhanced by Htc10-specific ligands. To our knowledge, this is the first description of binding specificity of a chemoreceptor that controls the activity of an associated diguanylate cyclase, opening the way for dynamic studies of the signaling behavior of this kind of sensory complex.Fil: Ramos Ricciutti, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaFil: Soldano, Anabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; ArgentinaFil: Herrera Seitz, Karina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; ArgentinaFil: Gasperotti, Ana Florencia. Ludwig Maximilians Universitat; AlemaniaFil: Boyko, Alexandra. Instituto Pasteur; FranciaFil: Jung, Kirsten. Ludwig Maximilians Universitat; AlemaniaFil: Bellinzoni, Marco. Instituto Pasteur; FranciaFil: Lisa, María Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. Plataforma de Biología Estructural y Metabolómica; ArgentinaFil: Studdert, Claudia Alicia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaWiley Blackwell Publishing, Inc2024-11info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/265492Ramos Ricciutti, Fernando; Soldano, Anabel; Herrera Seitz, Karina; Gasperotti, Ana Florencia; Boyko, Alexandra; et al.; The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives; Wiley Blackwell Publishing, Inc; Febs Journal; 292; 5; 11-2024; 1034-10511742-464XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.biorxiv.org/content/10.1101/2024.04.09.588698v1info:eu-repo/semantics/altIdentifier/doi/10.1111/febs.17320info:eu-repo/semantics/altIdentifier/url/https://febs.onlinelibrary.wiley.com/doi/full/10.1111/febs.17320info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:35:22Zoai:ri.conicet.gov.ar:11336/265492instacron: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 09:35:23.112CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
title The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
spellingShingle The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
Ramos Ricciutti, Fernando
HALOMONAS
CHEMORECEPTORS
GUANINE-BINDING
DOUBLE-CACHE SENSOR DOMAIN
title_short The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
title_full The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
title_fullStr The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
title_full_unstemmed The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
title_sort The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives
dc.creator.none.fl_str_mv Ramos Ricciutti, Fernando
Soldano, Anabel
Herrera Seitz, Karina
Gasperotti, Ana Florencia
Boyko, Alexandra
Jung, Kirsten
Bellinzoni, Marco
Lisa, María Natalia
Studdert, Claudia Alicia
author Ramos Ricciutti, Fernando
author_facet Ramos Ricciutti, Fernando
Soldano, Anabel
Herrera Seitz, Karina
Gasperotti, Ana Florencia
Boyko, Alexandra
Jung, Kirsten
Bellinzoni, Marco
Lisa, María Natalia
Studdert, Claudia Alicia
author_role author
author2 Soldano, Anabel
Herrera Seitz, Karina
Gasperotti, Ana Florencia
Boyko, Alexandra
Jung, Kirsten
Bellinzoni, Marco
Lisa, María Natalia
Studdert, Claudia Alicia
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv HALOMONAS
CHEMORECEPTORS
GUANINE-BINDING
DOUBLE-CACHE SENSOR DOMAIN
topic HALOMONAS
CHEMORECEPTORS
GUANINE-BINDING
DOUBLE-CACHE SENSOR DOMAIN
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The chemosensory pathway HtChe2 from the marine bacterium Halomonas titanicae KHS3 controls the activity of a diguanylate cyclase. Constitutive activation of this pathway results in colony morphology alterations and an increased ability to form biofilm. Such characteristics resemble the behavior of the Wsp pathway of Pseudomonas. In this work, we investigate the specificity of Htc10, the only chemoreceptor coded within the HtChe2 gene cluster. The purine derivatives guanine and hypoxanthine were identified as ligands of the recombinantly produced Htc10 ligand-binding domain, with dissociation constants in the micromolar range, and its structure was solved by X-ray protein crystallography. The sensor domain of Htc10 adopts a double Cache folding, with ligands bound to the membrane-distal pocket. A high-resolution structure of the occupied guanine-binding pocket allowed the identification of residues involved in ligand recognition. Such residues were validated by site-directed mutagenesis and isothermal titration calorimetry analyses of the protein variants. Moreover, heterologous expression of Htc10 in a Pseudomonas putida mutant lacking the native Wsp chemoreceptor promoted biofilm formation, a phenotype that was further enhanced by Htc10-specific ligands. To our knowledge, this is the first description of binding specificity of a chemoreceptor that controls the activity of an associated diguanylate cyclase, opening the way for dynamic studies of the signaling behavior of this kind of sensory complex.
Fil: Ramos Ricciutti, Fernando. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Soldano, Anabel. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Herrera Seitz, Karina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mar del Plata. Instituto de Investigaciones Biológicas. Universidad Nacional de Mar del Plata. Facultad de Ciencias Exactas y Naturales. Instituto de Investigaciones Biológicas; Argentina
Fil: Gasperotti, Ana Florencia. Ludwig Maximilians Universitat; Alemania
Fil: Boyko, Alexandra. Instituto Pasteur; Francia
Fil: Jung, Kirsten. Ludwig Maximilians Universitat; Alemania
Fil: Bellinzoni, Marco. Instituto Pasteur; Francia
Fil: Lisa, María Natalia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Rosario. Instituto de Biología Molecular y Celular de Rosario. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario; Argentina. Plataforma de Biología Estructural y Metabolómica; Argentina
Fil: Studdert, Claudia Alicia. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
description The chemosensory pathway HtChe2 from the marine bacterium Halomonas titanicae KHS3 controls the activity of a diguanylate cyclase. Constitutive activation of this pathway results in colony morphology alterations and an increased ability to form biofilm. Such characteristics resemble the behavior of the Wsp pathway of Pseudomonas. In this work, we investigate the specificity of Htc10, the only chemoreceptor coded within the HtChe2 gene cluster. The purine derivatives guanine and hypoxanthine were identified as ligands of the recombinantly produced Htc10 ligand-binding domain, with dissociation constants in the micromolar range, and its structure was solved by X-ray protein crystallography. The sensor domain of Htc10 adopts a double Cache folding, with ligands bound to the membrane-distal pocket. A high-resolution structure of the occupied guanine-binding pocket allowed the identification of residues involved in ligand recognition. Such residues were validated by site-directed mutagenesis and isothermal titration calorimetry analyses of the protein variants. Moreover, heterologous expression of Htc10 in a Pseudomonas putida mutant lacking the native Wsp chemoreceptor promoted biofilm formation, a phenotype that was further enhanced by Htc10-specific ligands. To our knowledge, this is the first description of binding specificity of a chemoreceptor that controls the activity of an associated diguanylate cyclase, opening the way for dynamic studies of the signaling behavior of this kind of sensory complex.
publishDate 2024
dc.date.none.fl_str_mv 2024-11
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/11336/265492
Ramos Ricciutti, Fernando; Soldano, Anabel; Herrera Seitz, Karina; Gasperotti, Ana Florencia; Boyko, Alexandra; et al.; The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives; Wiley Blackwell Publishing, Inc; Febs Journal; 292; 5; 11-2024; 1034-1051
1742-464X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/265492
identifier_str_mv Ramos Ricciutti, Fernando; Soldano, Anabel; Herrera Seitz, Karina; Gasperotti, Ana Florencia; Boyko, Alexandra; et al.; The chemoreceptor controlling the Wsp‐like transduction pathway in Halomonas titanicae KHS3 binds and responds to purine derivatives; Wiley Blackwell Publishing, Inc; Febs Journal; 292; 5; 11-2024; 1034-1051
1742-464X
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://www.biorxiv.org/content/10.1101/2024.04.09.588698v1
info:eu-repo/semantics/altIdentifier/doi/10.1111/febs.17320
info:eu-repo/semantics/altIdentifier/url/https://febs.onlinelibrary.wiley.com/doi/full/10.1111/febs.17320
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
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
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score 13.070432

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