Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom

The symbiosis between the diatom Hemiaulus hauckii and the heterocyst-forming cyanobacterium Richelia intracellularis makes an important contribution to new production in the world’s oceans, but its study is limited by short-term survival in the laboratory. In this symbiosis, R. intracellularis fixe...

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Detalles Bibliográficos
Autores: Flores García, Enrique, Romanovicz, Dwight K., Nieves Morión, Mercedes, Foster, R.A., Villareal, Tracy A.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2022
País:España
Institución:Universidad de Sevilla (US)
Repositorio:idUS. Depósito de Investigación de la Universidad de Sevilla
OAI Identifier:oai:idus.us.es:11441/131754
Acceso en línea:https://hdl.handle.net/11441/131754
https://doi.org/10.3389/fmicb.2022.799362
Access Level:acceso abierto
Palabra clave:cyanobacteria
diatom
Hemiaulus hauckii
heterocyst
membrane vesicles
Richelia intracellularis
symbiosis
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spelling Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a DiatomFlores García, EnriqueRomanovicz, Dwight K.Nieves Morión, MercedesFoster, R.A.Villareal, Tracy A.cyanobacteriadiatomHemiaulus hauckiiheterocystmembrane vesiclesRichelia intracellularissymbiosisThe symbiosis between the diatom Hemiaulus hauckii and the heterocyst-forming cyanobacterium Richelia intracellularis makes an important contribution to new production in the world’s oceans, but its study is limited by short-term survival in the laboratory. In this symbiosis, R. intracellularis fixes atmospheric dinitrogen in the heterocyst and provides H. hauckii with fixed nitrogen. Here, we conducted an electron microscopy study of H. hauckii and found that the filaments of the R. intracellularis symbiont, typically composed of one terminal heterocyst and three or four vegetative cells, are located in the diatom’s cytoplasm not enclosed by a host membrane. A second prokaryotic cell was also detected in the cytoplasm of H. hauckii, but observations were infrequent. The heterocysts of R. intracellularis differ from those of free-living heterocyst-forming cyanobacteria in that the specific components of the heterocyst envelope seem to be located in the periplasmic space instead of outside the outer membrane. This specialized arrangement of the heterocyst envelope and a possible association of the cyanobacterium with oxygen-respiring mitochondria may be important for protection of the nitrogen-fixing enzyme, nitrogenase, from photosynthetically produced oxygen. The cell envelope of the vegetative cells of R. intracellularis contained numerous membrane vesicles that resemble the outer-inner membrane vesicles of Gram-negative bacteria. These vesicles can export cytoplasmic material from the bacterial cell and, therefore, may represent a vehicle for transfer of fixed nitrogen from R. intracellularis to the diatom’s cytoplasm. The specific morphological features of R. intracellularis described here, together with its known streamlined genome, likely represent specific adaptations of this cyanobacterium to an intracellular lifestyle.Frontiers MediaBioquímica Vegetal y Biología Molecular2022info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttps://hdl.handle.net/11441/131754https://doi.org/10.3389/fmicb.2022.799362reponame:idUS. Depósito de Investigación de la Universidad de Sevillainstname:Universidad de Sevilla (US)InglésFrontiers in Microbiology, 13, 799362.https://dx.doi.org/10.3389/fmicb.2022.799362info:eu-repo/semantics/openAccessoai:idus.us.es:11441/1317542026-06-17T12:51:07Z
dc.title.none.fl_str_mv Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
title Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
spellingShingle Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
Flores García, Enrique
cyanobacteria
diatom
Hemiaulus hauckii
heterocyst
membrane vesicles
Richelia intracellularis
symbiosis
title_short Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
title_full Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
title_fullStr Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
title_full_unstemmed Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
title_sort Adaptation to an Intracellular Lifestyle by a Nitrogen-Fixing, Heterocyst-Forming Cyanobacterial Endosymbiont of a Diatom
dc.creator.none.fl_str_mv Flores García, Enrique
Romanovicz, Dwight K.
Nieves Morión, Mercedes
Foster, R.A.
Villareal, Tracy A.
author Flores García, Enrique
author_facet Flores García, Enrique
Romanovicz, Dwight K.
Nieves Morión, Mercedes
Foster, R.A.
Villareal, Tracy A.
author_role author
author2 Romanovicz, Dwight K.
Nieves Morión, Mercedes
Foster, R.A.
Villareal, Tracy A.
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Bioquímica Vegetal y Biología Molecular
dc.subject.none.fl_str_mv cyanobacteria
diatom
Hemiaulus hauckii
heterocyst
membrane vesicles
Richelia intracellularis
symbiosis
topic cyanobacteria
diatom
Hemiaulus hauckii
heterocyst
membrane vesicles
Richelia intracellularis
symbiosis
description The symbiosis between the diatom Hemiaulus hauckii and the heterocyst-forming cyanobacterium Richelia intracellularis makes an important contribution to new production in the world’s oceans, but its study is limited by short-term survival in the laboratory. In this symbiosis, R. intracellularis fixes atmospheric dinitrogen in the heterocyst and provides H. hauckii with fixed nitrogen. Here, we conducted an electron microscopy study of H. hauckii and found that the filaments of the R. intracellularis symbiont, typically composed of one terminal heterocyst and three or four vegetative cells, are located in the diatom’s cytoplasm not enclosed by a host membrane. A second prokaryotic cell was also detected in the cytoplasm of H. hauckii, but observations were infrequent. The heterocysts of R. intracellularis differ from those of free-living heterocyst-forming cyanobacteria in that the specific components of the heterocyst envelope seem to be located in the periplasmic space instead of outside the outer membrane. This specialized arrangement of the heterocyst envelope and a possible association of the cyanobacterium with oxygen-respiring mitochondria may be important for protection of the nitrogen-fixing enzyme, nitrogenase, from photosynthetically produced oxygen. The cell envelope of the vegetative cells of R. intracellularis contained numerous membrane vesicles that resemble the outer-inner membrane vesicles of Gram-negative bacteria. These vesicles can export cytoplasmic material from the bacterial cell and, therefore, may represent a vehicle for transfer of fixed nitrogen from R. intracellularis to the diatom’s cytoplasm. The specific morphological features of R. intracellularis described here, together with its known streamlined genome, likely represent specific adaptations of this cyanobacterium to an intracellular lifestyle.
publishDate 2022
dc.date.none.fl_str_mv 2022
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/11441/131754
https://doi.org/10.3389/fmicb.2022.799362
url https://hdl.handle.net/11441/131754
https://doi.org/10.3389/fmicb.2022.799362
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Frontiers in Microbiology, 13, 799362.
https://dx.doi.org/10.3389/fmicb.2022.799362
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 Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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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