Molecular Diffusion through Cyanobacterial Septal Junctions

ABSTRACT Heterocyst-forming cyanobacteria grow as filaments in which intercellular molecular exchange takes place. During the differentiation of N2-fixing heterocysts, regulators are transferred between cells. In the diazotrophic filament, vegetative cells that fix CO2 through oxygenic photosynthesi...

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Autores principales: Mercedes Nieves-Morión, Conrad W. Mullineaux, Enrique Flores
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:e2cc58f5289446ec91d01bd5d17e365e2021-11-15T15:51:07ZMolecular Diffusion through Cyanobacterial Septal Junctions10.1128/mBio.01756-162150-7511https://doaj.org/article/e2cc58f5289446ec91d01bd5d17e365e2017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01756-16https://doaj.org/toc/2150-7511ABSTRACT Heterocyst-forming cyanobacteria grow as filaments in which intercellular molecular exchange takes place. During the differentiation of N2-fixing heterocysts, regulators are transferred between cells. In the diazotrophic filament, vegetative cells that fix CO2 through oxygenic photosynthesis provide the heterocysts with reduced carbon and heterocysts provide the vegetative cells with fixed nitrogen. Intercellular molecular transfer has been traced with fluorescent markers, including calcein, 5-carboxyfluorescein, and the sucrose analogue esculin, which are observed to move down their concentration gradient. In this work, we used fluorescence recovery after photobleaching (FRAP) assays in the model heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 to measure the temperature dependence of intercellular transfer of fluorescent markers. We find that the transfer rate constants are directly proportional to the absolute temperature. This indicates that the “septal junctions” (formerly known as “microplasmodesmata”) linking the cells in the filament allow molecular exchange by simple diffusion, without any activated intermediate state. This constitutes a novel mechanism for molecular transfer across the bacterial cytoplasmic membrane, in addition to previously characterized mechanisms for active transport and facilitated diffusion. Cyanobacterial septal junctions are functionally analogous to the gap junctions of metazoans. IMPORTANCE Although bacteria are frequently considered just as unicellular organisms, there are bacteria that behave as true multicellular organisms. The heterocyst-forming cyanobacteria grow as filaments in which cells communicate. Intercellular molecular exchange is thought to be mediated by septal junctions. Here, we show that intercellular transfer of fluorescent markers in the cyanobacterial filament has the physical properties of simple diffusion. Thus, cyanobacterial septal junctions are functionally analogous to metazoan gap junctions, although their molecular components appear unrelated. Like metazoan gap junctions, the septal junctions of cyanobacteria allow the rapid intercellular exchange of small molecules, without stringent selectivity. Our finding expands the repertoire of mechanisms for molecular transfer across the plasma membrane in prokaryotes.Mercedes Nieves-MoriónConrad W. MullineauxEnrique FloresAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Mercedes Nieves-Morión
Conrad W. Mullineaux
Enrique Flores
Molecular Diffusion through Cyanobacterial Septal Junctions
description ABSTRACT Heterocyst-forming cyanobacteria grow as filaments in which intercellular molecular exchange takes place. During the differentiation of N2-fixing heterocysts, regulators are transferred between cells. In the diazotrophic filament, vegetative cells that fix CO2 through oxygenic photosynthesis provide the heterocysts with reduced carbon and heterocysts provide the vegetative cells with fixed nitrogen. Intercellular molecular transfer has been traced with fluorescent markers, including calcein, 5-carboxyfluorescein, and the sucrose analogue esculin, which are observed to move down their concentration gradient. In this work, we used fluorescence recovery after photobleaching (FRAP) assays in the model heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 to measure the temperature dependence of intercellular transfer of fluorescent markers. We find that the transfer rate constants are directly proportional to the absolute temperature. This indicates that the “septal junctions” (formerly known as “microplasmodesmata”) linking the cells in the filament allow molecular exchange by simple diffusion, without any activated intermediate state. This constitutes a novel mechanism for molecular transfer across the bacterial cytoplasmic membrane, in addition to previously characterized mechanisms for active transport and facilitated diffusion. Cyanobacterial septal junctions are functionally analogous to the gap junctions of metazoans. IMPORTANCE Although bacteria are frequently considered just as unicellular organisms, there are bacteria that behave as true multicellular organisms. The heterocyst-forming cyanobacteria grow as filaments in which cells communicate. Intercellular molecular exchange is thought to be mediated by septal junctions. Here, we show that intercellular transfer of fluorescent markers in the cyanobacterial filament has the physical properties of simple diffusion. Thus, cyanobacterial septal junctions are functionally analogous to metazoan gap junctions, although their molecular components appear unrelated. Like metazoan gap junctions, the septal junctions of cyanobacteria allow the rapid intercellular exchange of small molecules, without stringent selectivity. Our finding expands the repertoire of mechanisms for molecular transfer across the plasma membrane in prokaryotes.
format article
author Mercedes Nieves-Morión
Conrad W. Mullineaux
Enrique Flores
author_facet Mercedes Nieves-Morión
Conrad W. Mullineaux
Enrique Flores
author_sort Mercedes Nieves-Morión
title Molecular Diffusion through Cyanobacterial Septal Junctions
title_short Molecular Diffusion through Cyanobacterial Septal Junctions
title_full Molecular Diffusion through Cyanobacterial Septal Junctions
title_fullStr Molecular Diffusion through Cyanobacterial Septal Junctions
title_full_unstemmed Molecular Diffusion through Cyanobacterial Septal Junctions
title_sort molecular diffusion through cyanobacterial septal junctions
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/e2cc58f5289446ec91d01bd5d17e365e
work_keys_str_mv AT mercedesnievesmorion moleculardiffusionthroughcyanobacterialseptaljunctions
AT conradwmullineaux moleculardiffusionthroughcyanobacterialseptaljunctions
AT enriqueflores moleculardiffusionthroughcyanobacterialseptaljunctions
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