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Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae

Bacteria of the genus Streptomyces are a model system for bacterial multicellularity. Their mycelial life style involves the formation of long multinucleated hyphae during vegetative growth, with occasional cross-walls separating long compartments. Reproduction occurs by specialized aerial hyphae, w...

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Autores principales: Yagüe, Paula, Willemse, Joost, Koning, Roman I., Rioseras, Beatriz, López-García, María T., Gonzalez-Quiñonez, Nathaly, Lopez-Iglesias, Carmen, Shliaha, Pavel V., Rogowska-Wrzesinska, Adelina, Koster, Abraham J., Jensen, Ole N., van Wezel, Gilles P., Manteca, Ángel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4990651/
https://www.ncbi.nlm.nih.gov/pubmed/27514833
http://dx.doi.org/10.1038/ncomms12467
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author Yagüe, Paula
Willemse, Joost
Koning, Roman I.
Rioseras, Beatriz
López-García, María T.
Gonzalez-Quiñonez, Nathaly
Lopez-Iglesias, Carmen
Shliaha, Pavel V.
Rogowska-Wrzesinska, Adelina
Koster, Abraham J.
Jensen, Ole N.
van Wezel, Gilles P.
Manteca, Ángel
author_facet Yagüe, Paula
Willemse, Joost
Koning, Roman I.
Rioseras, Beatriz
López-García, María T.
Gonzalez-Quiñonez, Nathaly
Lopez-Iglesias, Carmen
Shliaha, Pavel V.
Rogowska-Wrzesinska, Adelina
Koster, Abraham J.
Jensen, Ole N.
van Wezel, Gilles P.
Manteca, Ángel
author_sort Yagüe, Paula
collection PubMed
description Bacteria of the genus Streptomyces are a model system for bacterial multicellularity. Their mycelial life style involves the formation of long multinucleated hyphae during vegetative growth, with occasional cross-walls separating long compartments. Reproduction occurs by specialized aerial hyphae, which differentiate into chains of uninucleoid spores. While the tubulin-like FtsZ protein is required for the formation of all peptidoglycan-based septa in Streptomyces, canonical divisome-dependent cell division only occurs during sporulation. Here we report extensive subcompartmentalization in young vegetative hyphae of Streptomyces coelicolor, whereby 1 μm compartments are formed by nucleic acid stain-impermeable barriers. These barriers possess the permeability properties of membranes and at least some of them are cross-membranes without detectable peptidoglycan. Z-ladders form during the early growth, but cross-membrane formation does not depend on FtsZ. Thus, a new level of hyphal organization is presented involving unprecedented high-frequency compartmentalization, which changes the old dogma that Streptomyces vegetative hyphae have scarce compartmentalization.
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spelling pubmed-49906512016-09-01 Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae Yagüe, Paula Willemse, Joost Koning, Roman I. Rioseras, Beatriz López-García, María T. Gonzalez-Quiñonez, Nathaly Lopez-Iglesias, Carmen Shliaha, Pavel V. Rogowska-Wrzesinska, Adelina Koster, Abraham J. Jensen, Ole N. van Wezel, Gilles P. Manteca, Ángel Nat Commun Article Bacteria of the genus Streptomyces are a model system for bacterial multicellularity. Their mycelial life style involves the formation of long multinucleated hyphae during vegetative growth, with occasional cross-walls separating long compartments. Reproduction occurs by specialized aerial hyphae, which differentiate into chains of uninucleoid spores. While the tubulin-like FtsZ protein is required for the formation of all peptidoglycan-based septa in Streptomyces, canonical divisome-dependent cell division only occurs during sporulation. Here we report extensive subcompartmentalization in young vegetative hyphae of Streptomyces coelicolor, whereby 1 μm compartments are formed by nucleic acid stain-impermeable barriers. These barriers possess the permeability properties of membranes and at least some of them are cross-membranes without detectable peptidoglycan. Z-ladders form during the early growth, but cross-membrane formation does not depend on FtsZ. Thus, a new level of hyphal organization is presented involving unprecedented high-frequency compartmentalization, which changes the old dogma that Streptomyces vegetative hyphae have scarce compartmentalization. Nature Publishing Group 2016-08-12 /pmc/articles/PMC4990651/ /pubmed/27514833 http://dx.doi.org/10.1038/ncomms12467 Text en Copyright © 2016, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Yagüe, Paula
Willemse, Joost
Koning, Roman I.
Rioseras, Beatriz
López-García, María T.
Gonzalez-Quiñonez, Nathaly
Lopez-Iglesias, Carmen
Shliaha, Pavel V.
Rogowska-Wrzesinska, Adelina
Koster, Abraham J.
Jensen, Ole N.
van Wezel, Gilles P.
Manteca, Ángel
Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title_full Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title_fullStr Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title_full_unstemmed Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title_short Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae
title_sort subcompartmentalization by cross-membranes during early growth of streptomyces hyphae
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4990651/
https://www.ncbi.nlm.nih.gov/pubmed/27514833
http://dx.doi.org/10.1038/ncomms12467
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