Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae

The water fern Azolla spp. harbors as an endobiont the N2-fixing, filamentous, heterocyst-forming cyanobacterium Nostoc azollae. N. azollae provides the fern with fixed nitrogen permitting its growth in nitrogen-poor environments. In the diazotrophic filaments of heterocyst-forming cyanobacteria, in...

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Autores: Sarasa-Buisan, Cristina, Nieves-Morión, Mercedes, Lindblad, Peter, Nierzwicki-Bauer, Sandra, Schluepmann, Henriette, Flores, Enrique
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/413814
Acceso en línea:http://hdl.handle.net/10261/413814
https://api.elsevier.com/content/abstract/scopus_id/105015768023
Access Level:acceso abierto
Palabra clave:Azolla
Nostoc azollae
Cyanobacteria
Intercellular communication
Septal junctions
Symbiosis
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spelling Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollaeSarasa-Buisan, CristinaNieves-Morión, MercedesLindblad, PeterNierzwicki-Bauer, SandraSchluepmann, HenrietteFlores, EnriqueAzollaNostoc azollaeCyanobacteriaIntercellular communicationSeptal junctionsSymbiosisThe water fern Azolla spp. harbors as an endobiont the N2-fixing, filamentous, heterocyst-forming cyanobacterium Nostoc azollae. N. azollae provides the fern with fixed nitrogen permitting its growth in nitrogen-poor environments. In the diazotrophic filaments of heterocyst-forming cyanobacteria, intercellular molecular exchange occurs in which heterocysts provide vegetative cells with fixed nitrogen and vegetative cells provide heterocysts with reduced carbon. Intercellular molecular exchange takes place by diffusion through septal junctions and can be probed by fluorescence recovery after photobleaching (FRAP) analysis with fluorescent markers such as calcein and 5-carboxyfluorescein. The septal junctions traverse the septal peptidoglycan (PG) through nanopores that can be visualized in isolated septal PG disks by electron microscopy. Here, we obtained from Azolla plants material containing the symbiotic cyanobacterium in a viable state and with different morphologies, including heterocyst-containing filaments. FRAP analysis showed effective transfer of the fluorescent markers between vegetative cells, as well as from vegetative cells to heterocysts. Interestingly, communicating and noncommunicating vegetative cells and heterocysts could be distinguished, showing conservation in the endobiont of a mechanism regulating the septal junctions. PG sacculi were also isolated and showed septal disks with arrays of nanopores that conform to those visualized in other heterocyst-forming cyanobacteria. However, a wider range of septal disk size was observed in N. azollae. In spite of its eroded genome, N. azollae maintains the intercellular communication system that is key for its growth as a multicellular organism. Additionally, labeling with the fluorescent sucrose analog esculin suggests sucrose as a source of reduced carbon for the endobiont.IMPORTANCEThe water fern Azolla constitutes a unique symbiotic system in which cyanobacterial endobionts capable of fixing atmospheric nitrogen provide the plant with the nitrogen needed for growth. This symbiosis is an important fertilizer for rice crops worldwide, thereby reducing the reliance on fossil fuel-derived nitrogen fertilizers. The symbiotic cyanobacterium, Nostoc azollae, is a heterocyst-forming strain in which a filament of cells is the organismic unit of growth. Here, we show that the intercellular molecular exchange function necessary for the multicellular behavior of the organism is conserved in the endobiotic N. azollae.The work was supported by the Gordon and Betty Moore Foundation grant no. 9355.Peer reviewedAmerican Society for MicrobiologyGordon and Betty Moore FoundationSarasa-Buisan, Cristina [0000-0002-1960-2672]Nieves-Morión, Mercedes [0000-0002-6615-0242]Lindblad, Peter [0000-0001-7256-0275]Nierzwicki-Bauer, Sandra [0000-0003-4058-4576]Schluepmann, Henriette [0000-0001-6171-3029]Flores, Enrique [0000-0001-7605-7343]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202620262025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/413814https://api.elsevier.com/content/abstract/scopus_id/105015768023reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)InglésThe underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://dx.doi.org/10.1128/mbio.01187-25http://dx.doi.org/10.1128/mbio.01187-25Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4138142026-05-22T06:33:51Z
dc.title.none.fl_str_mv Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
title Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
spellingShingle Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
Sarasa-Buisan, Cristina
Azolla
Nostoc azollae
Cyanobacteria
Intercellular communication
Septal junctions
Symbiosis
title_short Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
title_full Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
title_fullStr Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
title_full_unstemmed Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
title_sort Intercellular communication in the fern endosymbiotic cyanobacterium Nostoc azollae
dc.creator.none.fl_str_mv Sarasa-Buisan, Cristina
Nieves-Morión, Mercedes
Lindblad, Peter
Nierzwicki-Bauer, Sandra
Schluepmann, Henriette
Flores, Enrique
author Sarasa-Buisan, Cristina
author_facet Sarasa-Buisan, Cristina
Nieves-Morión, Mercedes
Lindblad, Peter
Nierzwicki-Bauer, Sandra
Schluepmann, Henriette
Flores, Enrique
author_role author
author2 Nieves-Morión, Mercedes
Lindblad, Peter
Nierzwicki-Bauer, Sandra
Schluepmann, Henriette
Flores, Enrique
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Gordon and Betty Moore Foundation
Sarasa-Buisan, Cristina [0000-0002-1960-2672]
Nieves-Morión, Mercedes [0000-0002-6615-0242]
Lindblad, Peter [0000-0001-7256-0275]
Nierzwicki-Bauer, Sandra [0000-0003-4058-4576]
Schluepmann, Henriette [0000-0001-6171-3029]
Flores, Enrique [0000-0001-7605-7343]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Azolla
Nostoc azollae
Cyanobacteria
Intercellular communication
Septal junctions
Symbiosis
topic Azolla
Nostoc azollae
Cyanobacteria
Intercellular communication
Septal junctions
Symbiosis
description The water fern Azolla spp. harbors as an endobiont the N2-fixing, filamentous, heterocyst-forming cyanobacterium Nostoc azollae. N. azollae provides the fern with fixed nitrogen permitting its growth in nitrogen-poor environments. In the diazotrophic filaments of heterocyst-forming cyanobacteria, intercellular molecular exchange occurs in which heterocysts provide vegetative cells with fixed nitrogen and vegetative cells provide heterocysts with reduced carbon. Intercellular molecular exchange takes place by diffusion through septal junctions and can be probed by fluorescence recovery after photobleaching (FRAP) analysis with fluorescent markers such as calcein and 5-carboxyfluorescein. The septal junctions traverse the septal peptidoglycan (PG) through nanopores that can be visualized in isolated septal PG disks by electron microscopy. Here, we obtained from Azolla plants material containing the symbiotic cyanobacterium in a viable state and with different morphologies, including heterocyst-containing filaments. FRAP analysis showed effective transfer of the fluorescent markers between vegetative cells, as well as from vegetative cells to heterocysts. Interestingly, communicating and noncommunicating vegetative cells and heterocysts could be distinguished, showing conservation in the endobiont of a mechanism regulating the septal junctions. PG sacculi were also isolated and showed septal disks with arrays of nanopores that conform to those visualized in other heterocyst-forming cyanobacteria. However, a wider range of septal disk size was observed in N. azollae. In spite of its eroded genome, N. azollae maintains the intercellular communication system that is key for its growth as a multicellular organism. Additionally, labeling with the fluorescent sucrose analog esculin suggests sucrose as a source of reduced carbon for the endobiont.IMPORTANCEThe water fern Azolla constitutes a unique symbiotic system in which cyanobacterial endobionts capable of fixing atmospheric nitrogen provide the plant with the nitrogen needed for growth. This symbiosis is an important fertilizer for rice crops worldwide, thereby reducing the reliance on fossil fuel-derived nitrogen fertilizers. The symbiotic cyanobacterium, Nostoc azollae, is a heterocyst-forming strain in which a filament of cells is the organismic unit of growth. Here, we show that the intercellular molecular exchange function necessary for the multicellular behavior of the organism is conserved in the endobiotic N. azollae.
publishDate 2025
dc.date.none.fl_str_mv 2025
2026
2026
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/10261/413814
https://api.elsevier.com/content/abstract/scopus_id/105015768023
url http://hdl.handle.net/10261/413814
https://api.elsevier.com/content/abstract/scopus_id/105015768023
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI http://dx.doi.org/10.1128/mbio.01187-25
http://dx.doi.org/10.1128/mbio.01187-25
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 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: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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