Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens

Autores
Hammerschmid, Dietmar; Germani, Francesca; Drusin, Salvador Iván; Fagnen, Charline; Schuster, Claudio David; Hoogewijs, David; Marti, Marcelo Adrian; Venien Bryan, Catherine; Moens, Luc; Van Doorslaer, Sabine; Sobott, Frank; Dewilde, Sylvia
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Globin-coupled sensors (GCS) usually consist of three domains: a sensor/globin, a linker, and a transmitter domain. The globin domain (GD), activated by ligand binding and/or redox change, induces an intramolecular signal transduction resulting in a response of the transmitter domain. Depending on the nature of the transmitter domain, GCSs can have different activities and functions, including adenylate and di-guanylate cyclase, histidine kinase activity, aerotaxis and/or oxygen sensing function. The gram-negative delta-proteobacterium Geobacter sulfurreducens expresses a protein with a GD covalently linked to a four transmembrane domain, classified, by sequence similarity, as GCS (GsGCS). While its GD is fully characterized, not so its transmembrane domain, which is rarely found in the globin superfamily. In the present work, GsGCS was characterized spectroscopically and by native ion mobility-mass spectrometry in combination with cryo-electron microscopy. Although lacking high resolution, the oligomeric state and the electron density map were valuable for further rational modeling of the full-length GsGCS structure. This model demonstrates that GsGCS forms a transmembrane domain-driven tetramer with minimal contact between the GDs and with the heme groups oriented outward. This organization makes an intramolecular signal transduction less likely. Our results, including the auto-oxidation rate and redox potential, suggest a potential role for GsGCS as redox sensor or in a membrane-bound e−/H+ transfer. As such, GsGCS might act as a player in connecting energy production to the oxidation of organic compounds and metal reduction. Database searches indicate that GDs linked to a four or seven helices transmembrane domain occur more frequently than expected.
Fil: Hammerschmid, Dietmar. Universiteit Antwerp; Bélgica
Fil: Germani, Francesca. Universiteit Antwerp; Bélgica
Fil: Drusin, Salvador Iván. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Fagnen, Charline. Sorbonne University; Francia
Fil: Schuster, Claudio David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Hoogewijs, David. University of Fribourg; Suiza
Fil: Marti, Marcelo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Venien Bryan, Catherine. Université Pierre et Marie Curie; Francia
Fil: Moens, Luc. Universiteit Antwerp; Bélgica
Fil: Van Doorslaer, Sabine. Universiteit Antwerp; Bélgica
Fil: Sobott, Frank. Universiteit Antwerp; Bélgica
Fil: Dewilde, Sylvia. Universiteit Antwerp; Bélgica
Materia
GEOBACTER SULFURREDUCENS
GLOBIN-COUPLED SENSOR
TRANSMEMBRANE DOMAIN
TRANSMEMBRANE-COUPLED GLOBINS
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:11336/173561
Acceder
id CONICETDig_ab1ee75230849130bc511611fc598d2a
oai_identifier_str oai:ri.conicet.gov.ar:11336/173561
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducensHammerschmid, DietmarGermani, FrancescaDrusin, Salvador IvánFagnen, CharlineSchuster, Claudio DavidHoogewijs, DavidMarti, Marcelo AdrianVenien Bryan, CatherineMoens, LucVan Doorslaer, SabineSobott, FrankDewilde, SylviaGEOBACTER SULFURREDUCENSGLOBIN-COUPLED SENSORTRANSMEMBRANE DOMAINTRANSMEMBRANE-COUPLED GLOBINShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Globin-coupled sensors (GCS) usually consist of three domains: a sensor/globin, a linker, and a transmitter domain. The globin domain (GD), activated by ligand binding and/or redox change, induces an intramolecular signal transduction resulting in a response of the transmitter domain. Depending on the nature of the transmitter domain, GCSs can have different activities and functions, including adenylate and di-guanylate cyclase, histidine kinase activity, aerotaxis and/or oxygen sensing function. The gram-negative delta-proteobacterium Geobacter sulfurreducens expresses a protein with a GD covalently linked to a four transmembrane domain, classified, by sequence similarity, as GCS (GsGCS). While its GD is fully characterized, not so its transmembrane domain, which is rarely found in the globin superfamily. In the present work, GsGCS was characterized spectroscopically and by native ion mobility-mass spectrometry in combination with cryo-electron microscopy. Although lacking high resolution, the oligomeric state and the electron density map were valuable for further rational modeling of the full-length GsGCS structure. This model demonstrates that GsGCS forms a transmembrane domain-driven tetramer with minimal contact between the GDs and with the heme groups oriented outward. This organization makes an intramolecular signal transduction less likely. Our results, including the auto-oxidation rate and redox potential, suggest a potential role for GsGCS as redox sensor or in a membrane-bound e−/H+ transfer. As such, GsGCS might act as a player in connecting energy production to the oxidation of organic compounds and metal reduction. Database searches indicate that GDs linked to a four or seven helices transmembrane domain occur more frequently than expected.Fil: Hammerschmid, Dietmar. Universiteit Antwerp; BélgicaFil: Germani, Francesca. Universiteit Antwerp; BélgicaFil: Drusin, Salvador Iván. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Fagnen, Charline. Sorbonne University; FranciaFil: Schuster, Claudio David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Hoogewijs, David. University of Fribourg; SuizaFil: Marti, Marcelo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Venien Bryan, Catherine. Université Pierre et Marie Curie; FranciaFil: Moens, Luc. Universiteit Antwerp; BélgicaFil: Van Doorslaer, Sabine. Universiteit Antwerp; BélgicaFil: Sobott, Frank. Universiteit Antwerp; BélgicaFil: Dewilde, Sylvia. Universiteit Antwerp; BélgicaElsevier2021-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/173561Hammerschmid, Dietmar; Germani, Francesca; Drusin, Salvador Iván; Fagnen, Charline; Schuster, Claudio David; et al.; Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens; Elsevier; Computational and Structural Biotechnology Journal; 19; 3-2021; 1874-18882001-0370CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S2001037021001033info:eu-repo/semantics/altIdentifier/doi/10.1016/j.csbj.2021.03.031info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:26:46Zoai:ri.conicet.gov.ar:11336/173561instacron: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 10:26:46.965CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
title Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
spellingShingle Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
Hammerschmid, Dietmar
GEOBACTER SULFURREDUCENS
GLOBIN-COUPLED SENSOR
TRANSMEMBRANE DOMAIN
TRANSMEMBRANE-COUPLED GLOBINS
title_short Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
title_full Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
title_fullStr Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
title_full_unstemmed Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
title_sort Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
dc.creator.none.fl_str_mv Hammerschmid, Dietmar
Germani, Francesca
Drusin, Salvador Iván
Fagnen, Charline
Schuster, Claudio David
Hoogewijs, David
Marti, Marcelo Adrian
Venien Bryan, Catherine
Moens, Luc
Van Doorslaer, Sabine
Sobott, Frank
Dewilde, Sylvia
author Hammerschmid, Dietmar
author_facet Hammerschmid, Dietmar
Germani, Francesca
Drusin, Salvador Iván
Fagnen, Charline
Schuster, Claudio David
Hoogewijs, David
Marti, Marcelo Adrian
Venien Bryan, Catherine
Moens, Luc
Van Doorslaer, Sabine
Sobott, Frank
Dewilde, Sylvia
author_role author
author2 Germani, Francesca
Drusin, Salvador Iván
Fagnen, Charline
Schuster, Claudio David
Hoogewijs, David
Marti, Marcelo Adrian
Venien Bryan, Catherine
Moens, Luc
Van Doorslaer, Sabine
Sobott, Frank
Dewilde, Sylvia
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv GEOBACTER SULFURREDUCENS
GLOBIN-COUPLED SENSOR
TRANSMEMBRANE DOMAIN
TRANSMEMBRANE-COUPLED GLOBINS
topic GEOBACTER SULFURREDUCENS
GLOBIN-COUPLED SENSOR
TRANSMEMBRANE DOMAIN
TRANSMEMBRANE-COUPLED GLOBINS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Globin-coupled sensors (GCS) usually consist of three domains: a sensor/globin, a linker, and a transmitter domain. The globin domain (GD), activated by ligand binding and/or redox change, induces an intramolecular signal transduction resulting in a response of the transmitter domain. Depending on the nature of the transmitter domain, GCSs can have different activities and functions, including adenylate and di-guanylate cyclase, histidine kinase activity, aerotaxis and/or oxygen sensing function. The gram-negative delta-proteobacterium Geobacter sulfurreducens expresses a protein with a GD covalently linked to a four transmembrane domain, classified, by sequence similarity, as GCS (GsGCS). While its GD is fully characterized, not so its transmembrane domain, which is rarely found in the globin superfamily. In the present work, GsGCS was characterized spectroscopically and by native ion mobility-mass spectrometry in combination with cryo-electron microscopy. Although lacking high resolution, the oligomeric state and the electron density map were valuable for further rational modeling of the full-length GsGCS structure. This model demonstrates that GsGCS forms a transmembrane domain-driven tetramer with minimal contact between the GDs and with the heme groups oriented outward. This organization makes an intramolecular signal transduction less likely. Our results, including the auto-oxidation rate and redox potential, suggest a potential role for GsGCS as redox sensor or in a membrane-bound e−/H+ transfer. As such, GsGCS might act as a player in connecting energy production to the oxidation of organic compounds and metal reduction. Database searches indicate that GDs linked to a four or seven helices transmembrane domain occur more frequently than expected.
Fil: Hammerschmid, Dietmar. Universiteit Antwerp; Bélgica
Fil: Germani, Francesca. Universiteit Antwerp; Bélgica
Fil: Drusin, Salvador Iván. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Fagnen, Charline. Sorbonne University; Francia
Fil: Schuster, Claudio David. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Hoogewijs, David. University of Fribourg; Suiza
Fil: Marti, Marcelo Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales; Argentina
Fil: Venien Bryan, Catherine. Université Pierre et Marie Curie; Francia
Fil: Moens, Luc. Universiteit Antwerp; Bélgica
Fil: Van Doorslaer, Sabine. Universiteit Antwerp; Bélgica
Fil: Sobott, Frank. Universiteit Antwerp; Bélgica
Fil: Dewilde, Sylvia. Universiteit Antwerp; Bélgica
description Globin-coupled sensors (GCS) usually consist of three domains: a sensor/globin, a linker, and a transmitter domain. The globin domain (GD), activated by ligand binding and/or redox change, induces an intramolecular signal transduction resulting in a response of the transmitter domain. Depending on the nature of the transmitter domain, GCSs can have different activities and functions, including adenylate and di-guanylate cyclase, histidine kinase activity, aerotaxis and/or oxygen sensing function. The gram-negative delta-proteobacterium Geobacter sulfurreducens expresses a protein with a GD covalently linked to a four transmembrane domain, classified, by sequence similarity, as GCS (GsGCS). While its GD is fully characterized, not so its transmembrane domain, which is rarely found in the globin superfamily. In the present work, GsGCS was characterized spectroscopically and by native ion mobility-mass spectrometry in combination with cryo-electron microscopy. Although lacking high resolution, the oligomeric state and the electron density map were valuable for further rational modeling of the full-length GsGCS structure. This model demonstrates that GsGCS forms a transmembrane domain-driven tetramer with minimal contact between the GDs and with the heme groups oriented outward. This organization makes an intramolecular signal transduction less likely. Our results, including the auto-oxidation rate and redox potential, suggest a potential role for GsGCS as redox sensor or in a membrane-bound e−/H+ transfer. As such, GsGCS might act as a player in connecting energy production to the oxidation of organic compounds and metal reduction. Database searches indicate that GDs linked to a four or seven helices transmembrane domain occur more frequently than expected.
publishDate 2021
dc.date.none.fl_str_mv 2021-03
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/11336/173561
Hammerschmid, Dietmar; Germani, Francesca; Drusin, Salvador Iván; Fagnen, Charline; Schuster, Claudio David; et al.; Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens; Elsevier; Computational and Structural Biotechnology Journal; 19; 3-2021; 1874-1888
2001-0370
CONICET Digital
CONICET
url http://hdl.handle.net/11336/173561
identifier_str_mv Hammerschmid, Dietmar; Germani, Francesca; Drusin, Salvador Iván; Fagnen, Charline; Schuster, Claudio David; et al.; Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens; Elsevier; Computational and Structural Biotechnology Journal; 19; 3-2021; 1874-1888
2001-0370
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://linkinghub.elsevier.com/retrieve/pii/S2001037021001033
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.csbj.2021.03.031
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
dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
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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