SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120

Anabaena sp. PCC 7120 grows by forming filaments of communicating cells and is considered a paradigm of bacterial multicellularity. Molecular exchanges between contiguous cells in the filament take place through multiprotein channels that traverse the septal peptidoglycan through nanopores connectin...

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Autores: Velázquez Suárez, Cristina, Springstein, B. L., Nieves Morión, M., Helbig, A. O., Kieninger, A. K., Maldener, I., Nürnberg, D. J., Stucken, K., Luque, I., Dagan, T., Herrero, A.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2002
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/177220
Acceso en línea:https://hdl.handle.net/11441/177220
https://doi.org/10.1128/mbio.00983-23
Access Level:acceso abierto
Palabra clave:Coiled-coil-rich proteins
Divisome-dependent localization
Filamentous cyanobacteria
Septal peptidoglycan nanopores
Septal proteins
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spelling SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120Velázquez Suárez, CristinaSpringstein, B. L.Nieves Morión, M.Helbig, A. O.Kieninger, A. K.Maldener, I.Nürnberg, D. J.Stucken, K.Luque, I.Dagan, T.Herrero, A.Coiled-coil-rich proteinsDivisome-dependent localizationFilamentous cyanobacteriaSeptal peptidoglycan nanoporesSeptal proteinsAnabaena sp. PCC 7120 grows by forming filaments of communicating cells and is considered a paradigm of bacterial multicellularity. Molecular exchanges between contiguous cells in the filament take place through multiprotein channels that traverse the septal peptidoglycan through nanopores connecting their cytoplasms. Besides, the septal-junction complexes contribute to strengthen the filament. In search for proteins with coiled-coil domains that could provide for cytoskeletal functions in Anabaena, we identified SepT (All2460). SepT is characteristic of the phylogenetic clade of filamentous cyanobacteria with the ability to undergo cell differentiation. SepT-GFP fusions indicate that the protein is located at the cell periphery and, conspicuously, in the intercellular septa. During cell division, the protein is found at midcell resembling the position of the divisome. The bacterial adenylate cyclase two-hybrid analysis shows SepT interactions with itself and putative elongasome (MreB, RodA), divisome (FtsW, SepF, ZipN), and septal-junction (SepJ)-related proteins. Thus, SepT appears to rely on the divisome for localization at mature intercellular septa to form part of intercellular protein complexes. Two independently obtained mutants lacking SepT showed alterations in cell size and impaired septal and peripheral peptidoglycan incorporation during cell growth and division. Notably, both mutants showed conspicuous alterations in the array of nanopores present in the intercellular peptidoglycan disks, including aberrant nanopore morphology, number, and distribution. SepT appears, therefore, to be involved in the control of peptidoglycan growth and the formation of cell-cell communication structures that are at the basis of the multicellular character of this group of cyanobacteria. IMPORTANCE Multicellular organization is a requirement for the development of complex organisms, and filamentous cyanobacteria such as Anabaena represent a paradigmatic case of bacterial multicellularity. The Anabaena filament can include hundreds of communicated cells that exchange nutrients and regulators and, depending on environmental conditions, can include different cell types specialized in distinct biological functions. Hence, the specific features of the Anabaena filament and how they are propagated during cell division represent outstanding biological issues. Here, we studied SepT, a novel coiled-coil-rich protein of Anabaena that is located in the intercellular septa and influences the formation of the septal specialized structures that allow communication between neighboring cells along the filament, a fundamental trait for the performance of Anabaena as a multicellular organism.American Society for MicrobiologyGenéticaMinisterio de Ciencia e Innovación (MICIN). EspañaJunta de AndalucíaGerman Science Foundation (DFG)2002info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/177220https://doi.org/10.1128/mbio.00983-23reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésMBIO, 14 (5), e00983-23.PID2020-118595GB-100P20-00032STU513/2-1NU 421/1https://doi.org/10.1128/mbio.00983-23info:eu-repo/semantics/openAccessoai:idus.us.es:11441/1772202026-06-17T12:51:07Z
dc.title.none.fl_str_mv SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
title SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
spellingShingle SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
Velázquez Suárez, Cristina
Coiled-coil-rich proteins
Divisome-dependent localization
Filamentous cyanobacteria
Septal peptidoglycan nanopores
Septal proteins
title_short SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
title_full SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
title_fullStr SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
title_full_unstemmed SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
title_sort SepT, A Novel Protein Specific to Multicellular Cyanobacteria, Influences Peptidoglycan Growth and Septal Nanopore Formation in Anabaena sp. PCC 7120
dc.creator.none.fl_str_mv Velázquez Suárez, Cristina
Springstein, B. L.
Nieves Morión, M.
Helbig, A. O.
Kieninger, A. K.
Maldener, I.
Nürnberg, D. J.
Stucken, K.
Luque, I.
Dagan, T.
Herrero, A.
author Velázquez Suárez, Cristina
author_facet Velázquez Suárez, Cristina
Springstein, B. L.
Nieves Morión, M.
Helbig, A. O.
Kieninger, A. K.
Maldener, I.
Nürnberg, D. J.
Stucken, K.
Luque, I.
Dagan, T.
Herrero, A.
author_role author
author2 Springstein, B. L.
Nieves Morión, M.
Helbig, A. O.
Kieninger, A. K.
Maldener, I.
Nürnberg, D. J.
Stucken, K.
Luque, I.
Dagan, T.
Herrero, A.
author2_role author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Genética
Ministerio de Ciencia e Innovación (MICIN). España
Junta de Andalucía
German Science Foundation (DFG)
dc.subject.none.fl_str_mv Coiled-coil-rich proteins
Divisome-dependent localization
Filamentous cyanobacteria
Septal peptidoglycan nanopores
Septal proteins
topic Coiled-coil-rich proteins
Divisome-dependent localization
Filamentous cyanobacteria
Septal peptidoglycan nanopores
Septal proteins
description Anabaena sp. PCC 7120 grows by forming filaments of communicating cells and is considered a paradigm of bacterial multicellularity. Molecular exchanges between contiguous cells in the filament take place through multiprotein channels that traverse the septal peptidoglycan through nanopores connecting their cytoplasms. Besides, the septal-junction complexes contribute to strengthen the filament. In search for proteins with coiled-coil domains that could provide for cytoskeletal functions in Anabaena, we identified SepT (All2460). SepT is characteristic of the phylogenetic clade of filamentous cyanobacteria with the ability to undergo cell differentiation. SepT-GFP fusions indicate that the protein is located at the cell periphery and, conspicuously, in the intercellular septa. During cell division, the protein is found at midcell resembling the position of the divisome. The bacterial adenylate cyclase two-hybrid analysis shows SepT interactions with itself and putative elongasome (MreB, RodA), divisome (FtsW, SepF, ZipN), and septal-junction (SepJ)-related proteins. Thus, SepT appears to rely on the divisome for localization at mature intercellular septa to form part of intercellular protein complexes. Two independently obtained mutants lacking SepT showed alterations in cell size and impaired septal and peripheral peptidoglycan incorporation during cell growth and division. Notably, both mutants showed conspicuous alterations in the array of nanopores present in the intercellular peptidoglycan disks, including aberrant nanopore morphology, number, and distribution. SepT appears, therefore, to be involved in the control of peptidoglycan growth and the formation of cell-cell communication structures that are at the basis of the multicellular character of this group of cyanobacteria. IMPORTANCE Multicellular organization is a requirement for the development of complex organisms, and filamentous cyanobacteria such as Anabaena represent a paradigmatic case of bacterial multicellularity. The Anabaena filament can include hundreds of communicated cells that exchange nutrients and regulators and, depending on environmental conditions, can include different cell types specialized in distinct biological functions. Hence, the specific features of the Anabaena filament and how they are propagated during cell division represent outstanding biological issues. Here, we studied SepT, a novel coiled-coil-rich protein of Anabaena that is located in the intercellular septa and influences the formation of the septal specialized structures that allow communication between neighboring cells along the filament, a fundamental trait for the performance of Anabaena as a multicellular organism.
publishDate 2002
dc.date.none.fl_str_mv 2002
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/11441/177220
https://doi.org/10.1128/mbio.00983-23
url https://hdl.handle.net/11441/177220
https://doi.org/10.1128/mbio.00983-23
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv MBIO, 14 (5), e00983-23.
PID2020-118595GB-100
P20-00032
STU513/2-1
NU 421/1
https://doi.org/10.1128/mbio.00983-23
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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:idUS. Depósito de Investigación de la Universidad de Sevilla
instname:Universidad de Sevilla (US)
instname_str Universidad de Sevilla (US)
reponame_str idUS. Depósito de Investigación de la Universidad de Sevilla
collection idUS. Depósito de Investigación de la Universidad de Sevilla
repository.name.fl_str_mv
repository.mail.fl_str_mv
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