SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120
ABSTRACT 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...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mBio |
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.00983-23 |
| _version_ | 1827150309765414912 |
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| author | Cristina Velázquez-Suárez Benjamin L. Springstein Mercedes Nieves-Morión Andreas O. Helbig Ann-Katrin Kieninger Iris Maldener Dennis J. Nürnberg Karina Stucken Ignacio Luque Tal Dagan Antonia Herrero |
| author_facet | Cristina Velázquez-Suárez Benjamin L. Springstein Mercedes Nieves-Morión Andreas O. Helbig Ann-Katrin Kieninger Iris Maldener Dennis J. Nürnberg Karina Stucken Ignacio Luque Tal Dagan Antonia Herrero |
| author_sort | Cristina Velázquez-Suárez |
| collection | DOAJ |
| description | ABSTRACT 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. |
| first_indexed | 2024-03-11T08:30:29Z |
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| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2025-03-20T21:32:02Z |
| publishDate | 2023-10-01 |
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| series | mBio |
| spelling | doaj.art-7f4f866a4ccd4189876f1721362a01ec2024-08-11T18:20:46ZengAmerican Society for MicrobiologymBio2150-75112023-10-0114510.1128/mbio.00983-23SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120Cristina Velázquez-Suárez0Benjamin L. Springstein1Mercedes Nieves-Morión2Andreas O. Helbig3Ann-Katrin Kieninger4Iris Maldener5Dennis J. Nürnberg6Karina Stucken7Ignacio Luque8Tal Dagan9Antonia Herrero10Instituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla , Seville, SpainInstitute of General Microbiology, Kiel University , Kiel, GermanyInstituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla , Seville, SpainAG Proteomics & Bioanalytics, Institute for Experimental Medicine, Christian-Albrechts-Universität zu Kiel , Kiel, GermanyDepartment of Microbiology/Organismic Interactions, University of Tübingen , Tübingen, GermanyDepartment of Microbiology/Organismic Interactions, University of Tübingen , Tübingen, GermanyInstitute of Experimental Physics and Dahlem Centre of Plant Sciences, Free University of Berlin , Berlin, GermanyDepartment of Food Engineering, Universidad de La Serena , La Serena, ChileInstituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla , Seville, SpainInstitute of General Microbiology, Kiel University , Kiel, GermanyInstituto de Bioquímica Vegetal y Fotosíntesis, CSIC and Universidad de Sevilla , Seville, SpainABSTRACT 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.https://journals.asm.org/doi/10.1128/mbio.00983-23coiled-coil-rich proteinsdivisome-dependent localizationfilamentous cyanobacteriaseptal peptidoglycan nanoporesseptal proteins |
| spellingShingle | Cristina Velázquez-Suárez Benjamin L. Springstein Mercedes Nieves-Morión Andreas O. Helbig Ann-Katrin Kieninger Iris Maldener Dennis J. Nürnberg Karina Stucken Ignacio Luque Tal Dagan Antonia Herrero SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120 mBio coiled-coil-rich proteins divisome-dependent localization filamentous cyanobacteria septal peptidoglycan nanopores septal proteins |
| title | 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_short | 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 |
| topic | coiled-coil-rich proteins divisome-dependent localization filamentous cyanobacteria septal peptidoglycan nanopores septal proteins |
| url | https://journals.asm.org/doi/10.1128/mbio.00983-23 |
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