Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

In filamentous heterocyst-forming (N2-fixing) cyanobacteria, septal junctions join adjacent cells, mediating intercellular communication, and are thought to traverse the septal peptidoglycan through nanopores. Fluorescence recovery after photobleaching (FRAP) analysis with the fluorescent marker cal...

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Autores: Arévalo, Sergio, Nenninger, Anja, Nieves-Morión, Mercedes, Herrero, Antonia, Mullineaux, Conrad W., Flores, Enrique
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2021
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/228698
Acceso en línea:http://hdl.handle.net/10261/228698
Access Level:acceso abierto
Palabra clave:Cyanobacteria
Intercellular communication
Septal junctions
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spelling Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium AnabaenaArévalo, SergioNenninger, AnjaNieves-Morión, MercedesHerrero, AntoniaMullineaux, Conrad W.Flores, EnriqueCyanobacteriaIntercellular communicationSeptal junctionsIn filamentous heterocyst-forming (N2-fixing) cyanobacteria, septal junctions join adjacent cells, mediating intercellular communication, and are thought to traverse the septal peptidoglycan through nanopores. Fluorescence recovery after photobleaching (FRAP) analysis with the fluorescent marker calcein showed that cultures of Anabaena sp. strain PCC 7120 grown in the presence of combined nitrogen contained a substantial fraction of noncommunicating cells (58% and 80% of the tested vegetative cells in nitrate- and ammonium-grown cultures, respectively), whereas cultures induced for nitrogen fixation contained far fewer noncommunicating cells (16%). A single filament could have communicating and noncommunicating cells. These observations indicate that all (or most of) the septal junctions in a cell can be coordinately regulated and are coherent with the need for intercellular communication, especially under diazotrophic conditions. Consistently, intercellular exchange was observed to increase in response to N deprivation and to decrease rapidly in response to the presence of ammonium in the medium or to nitrate assimilation. Proteins involved in the formation of septal junctions have been identified in Anabaena and include SepJ, FraC, and FraD. Here, we reevaluated rates of intercellular transfer of calcein and the number of nanopores in mutants lacking these proteins and found a strong positive correlation between the two parameters only in cultures induced for nitrogen fixation. Thus, whereas the presence of a substantial number of noncommunicating cells appears to impair the correlation, data obtained in diazotrophic cultures support the idea that the nanopores are the structures that hold the septal junctions.Peer reviewedAmerican Society for MicrobiologyConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202120212021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/228698reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://doi.org/10.1128/mSphere .01091-20.Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2286982026-05-22T06:33:51Z
dc.title.none.fl_str_mv Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
title Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
spellingShingle Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
Arévalo, Sergio
Cyanobacteria
Intercellular communication
Septal junctions
title_short Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
title_full Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
title_fullStr Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
title_full_unstemmed Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
title_sort Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena
dc.creator.none.fl_str_mv Arévalo, Sergio
Nenninger, Anja
Nieves-Morión, Mercedes
Herrero, Antonia
Mullineaux, Conrad W.
Flores, Enrique
author Arévalo, Sergio
author_facet Arévalo, Sergio
Nenninger, Anja
Nieves-Morión, Mercedes
Herrero, Antonia
Mullineaux, Conrad W.
Flores, Enrique
author_role author
author2 Nenninger, Anja
Nieves-Morión, Mercedes
Herrero, Antonia
Mullineaux, Conrad W.
Flores, Enrique
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Cyanobacteria
Intercellular communication
Septal junctions
topic Cyanobacteria
Intercellular communication
Septal junctions
description In filamentous heterocyst-forming (N2-fixing) cyanobacteria, septal junctions join adjacent cells, mediating intercellular communication, and are thought to traverse the septal peptidoglycan through nanopores. Fluorescence recovery after photobleaching (FRAP) analysis with the fluorescent marker calcein showed that cultures of Anabaena sp. strain PCC 7120 grown in the presence of combined nitrogen contained a substantial fraction of noncommunicating cells (58% and 80% of the tested vegetative cells in nitrate- and ammonium-grown cultures, respectively), whereas cultures induced for nitrogen fixation contained far fewer noncommunicating cells (16%). A single filament could have communicating and noncommunicating cells. These observations indicate that all (or most of) the septal junctions in a cell can be coordinately regulated and are coherent with the need for intercellular communication, especially under diazotrophic conditions. Consistently, intercellular exchange was observed to increase in response to N deprivation and to decrease rapidly in response to the presence of ammonium in the medium or to nitrate assimilation. Proteins involved in the formation of septal junctions have been identified in Anabaena and include SepJ, FraC, and FraD. Here, we reevaluated rates of intercellular transfer of calcein and the number of nanopores in mutants lacking these proteins and found a strong positive correlation between the two parameters only in cultures induced for nitrogen fixation. Thus, whereas the presence of a substantial number of noncommunicating cells appears to impair the correlation, data obtained in diazotrophic cultures support the idea that the nanopores are the structures that hold the septal junctions.
publishDate 2021
dc.date.none.fl_str_mv 2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/228698
url http://hdl.handle.net/10261/228698
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv https://doi.org/10.1128/mSphere .01091-20.
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
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:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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