Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens
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 t...
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| Format: | Article |
| Language: | English |
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Elsevier
2021-01-01
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| Series: | Computational and Structural Biotechnology Journal |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2001037021001033 |
| _version_ | 1818979585460535296 |
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| author | Dietmar Hammerschmid Francesca Germani Salvador I. Drusin Charline Fagnen Claudio D. Schuster David Hoogewijs Marcelo A. Marti Catherine Venien-Bryan Luc Moens Sabine Van Doorslaer Frank Sobott Sylvia Dewilde |
| author_facet | Dietmar Hammerschmid Francesca Germani Salvador I. Drusin Charline Fagnen Claudio D. Schuster David Hoogewijs Marcelo A. Marti Catherine Venien-Bryan Luc Moens Sabine Van Doorslaer Frank Sobott Sylvia Dewilde |
| author_sort | Dietmar Hammerschmid |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-20T17:01:52Z |
| format | Article |
| id | doaj.art-02c5fe5a57b54d7b85a3d980154a4e0b |
| institution | Directory Open Access Journal |
| issn | 2001-0370 |
| language | English |
| last_indexed | 2024-12-20T17:01:52Z |
| publishDate | 2021-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Computational and Structural Biotechnology Journal |
| spelling | doaj.art-02c5fe5a57b54d7b85a3d980154a4e0b2022-12-21T19:32:30ZengElsevierComputational and Structural Biotechnology Journal2001-03702021-01-011918741888Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducensDietmar Hammerschmid0Francesca Germani1Salvador I. Drusin2Charline Fagnen3Claudio D. Schuster4David Hoogewijs5Marcelo A. Marti6Catherine Venien-Bryan7Luc Moens8Sabine Van Doorslaer9Frank Sobott10Sylvia Dewilde11Proteinchemistry, Proteomics and Epigenetic Signalling, Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium; Biomolecular & Analytical Mass Spectrometry, Department of Chemistry, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, BelgiumProteinchemistry, Proteomics and Epigenetic Signalling, Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, BelgiumDepartamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEyN-UBA) e Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN) CONICET, Pabellòn 2 de Ciudad Universitaria, Ciudad de Buenos Aires C1428EHA, ArgentinaSorbonne Université, UMR 7590, CNRS, Muséum National d’Histoire Naturelle, Institut de Minéralogie, Physique des Matériaux et Cosmochimie, IMPMC, 75005 Paris, FranceDepartamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEyN-UBA) e Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN) CONICET, Pabellòn 2 de Ciudad Universitaria, Ciudad de Buenos Aires C1428EHA, ArgentinaSection of Medicine, Department of Endocrinology, Metabolism and Cardiovascular System, University of Fribourg, SwitzerlandDepartamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires (FCEyN-UBA) e Instituto de Química Biológica de la Facultad de Ciencias Exactas y Naturales (IQUIBICEN) CONICET, Pabellòn 2 de Ciudad Universitaria, Ciudad de Buenos Aires C1428EHA, ArgentinaSorbonne Université, UMR 7590, CNRS, Muséum National d’Histoire Naturelle, Institut de Minéralogie, Physique des Matériaux et Cosmochimie, IMPMC, 75005 Paris, FranceProteinchemistry, Proteomics and Epigenetic Signalling, Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, BelgiumBiophysics and Biomedical Physics, Department of Chemistry, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, Belgium; Corresponding authors.Biomolecular & Analytical Mass Spectrometry, Department of Chemistry, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerp, Belgium; Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds LS2 9JT, United Kingdom; School of Molecular and Cellular Biology, University of Leeds, LS2 9JT, United Kingdom; Corresponding authors.Proteinchemistry, Proteomics and Epigenetic Signalling, Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, 2610 Wilrijk, BelgiumGlobin-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.http://www.sciencedirect.com/science/article/pii/S2001037021001033Globin-coupled sensorGeobacter sulfurreducensTransmembrane domainTransmembrane-coupled globins |
| spellingShingle | Dietmar Hammerschmid Francesca Germani Salvador I. Drusin Charline Fagnen Claudio D. Schuster David Hoogewijs Marcelo A. Marti Catherine Venien-Bryan Luc Moens Sabine Van Doorslaer Frank Sobott Sylvia Dewilde Structural modeling of a novel membrane-bound globin-coupled sensor in Geobacter sulfurreducens Computational and Structural Biotechnology Journal Globin-coupled sensor Geobacter sulfurreducens Transmembrane domain Transmembrane-coupled globins |
| title | 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_short | 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 |
| topic | Globin-coupled sensor Geobacter sulfurreducens Transmembrane domain Transmembrane-coupled globins |
| url | http://www.sciencedirect.com/science/article/pii/S2001037021001033 |
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