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Endocytosis-like DNA uptake by cell wall-deficient bacteria

Horizontal gene transfer in bacteria is widely believed to occur via conjugation, transduction and transformation. These mechanisms facilitate the passage of DNA across the protective cell wall using sophisticated machinery. Here, we report that cell wall-deficient bacteria can engulf DNA and other...

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Autores principales: Kapteijn, Renée, Shitut, Shraddha, Aschmann, Dennis, Zhang, Le, de Beer, Marit, Daviran, Deniz, Roverts, Rona, Akiva, Anat, van Wezel, Gilles P., Kros, Alexander, Claessen, Dennis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9500057/
https://www.ncbi.nlm.nih.gov/pubmed/36138004
http://dx.doi.org/10.1038/s41467-022-33054-w
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author Kapteijn, Renée
Shitut, Shraddha
Aschmann, Dennis
Zhang, Le
de Beer, Marit
Daviran, Deniz
Roverts, Rona
Akiva, Anat
van Wezel, Gilles P.
Kros, Alexander
Claessen, Dennis
author_facet Kapteijn, Renée
Shitut, Shraddha
Aschmann, Dennis
Zhang, Le
de Beer, Marit
Daviran, Deniz
Roverts, Rona
Akiva, Anat
van Wezel, Gilles P.
Kros, Alexander
Claessen, Dennis
author_sort Kapteijn, Renée
collection PubMed
description Horizontal gene transfer in bacteria is widely believed to occur via conjugation, transduction and transformation. These mechanisms facilitate the passage of DNA across the protective cell wall using sophisticated machinery. Here, we report that cell wall-deficient bacteria can engulf DNA and other extracellular material via an endocytosis-like process. Specifically, we show that L-forms of the filamentous actinomycete Kitasatospora viridifaciens can take up plasmid DNA, polysaccharides (dextran) and 150-nm lipid nanoparticles. The process involves invagination of the cytoplasmic membrane, leading to formation of intracellular vesicles that encapsulate extracellular material. DNA uptake is not affected by deletion of genes homologous to comEC and comEA, which are required for natural transformation in other species. However, uptake is inhibited by sodium azide or incubation at 4 °C, suggesting the process is energy-dependent. The encapsulated materials are released into the cytoplasm upon degradation of the vesicle membrane. Given that cell wall-deficient bacteria are considered a model for early life forms, our work reveals a possible mechanism for primordial cells to acquire food or genetic material before invention of the bacterial cell wall.
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spelling pubmed-95000572022-09-24 Endocytosis-like DNA uptake by cell wall-deficient bacteria Kapteijn, Renée Shitut, Shraddha Aschmann, Dennis Zhang, Le de Beer, Marit Daviran, Deniz Roverts, Rona Akiva, Anat van Wezel, Gilles P. Kros, Alexander Claessen, Dennis Nat Commun Article Horizontal gene transfer in bacteria is widely believed to occur via conjugation, transduction and transformation. These mechanisms facilitate the passage of DNA across the protective cell wall using sophisticated machinery. Here, we report that cell wall-deficient bacteria can engulf DNA and other extracellular material via an endocytosis-like process. Specifically, we show that L-forms of the filamentous actinomycete Kitasatospora viridifaciens can take up plasmid DNA, polysaccharides (dextran) and 150-nm lipid nanoparticles. The process involves invagination of the cytoplasmic membrane, leading to formation of intracellular vesicles that encapsulate extracellular material. DNA uptake is not affected by deletion of genes homologous to comEC and comEA, which are required for natural transformation in other species. However, uptake is inhibited by sodium azide or incubation at 4 °C, suggesting the process is energy-dependent. The encapsulated materials are released into the cytoplasm upon degradation of the vesicle membrane. Given that cell wall-deficient bacteria are considered a model for early life forms, our work reveals a possible mechanism for primordial cells to acquire food or genetic material before invention of the bacterial cell wall. Nature Publishing Group UK 2022-09-22 /pmc/articles/PMC9500057/ /pubmed/36138004 http://dx.doi.org/10.1038/s41467-022-33054-w Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kapteijn, Renée
Shitut, Shraddha
Aschmann, Dennis
Zhang, Le
de Beer, Marit
Daviran, Deniz
Roverts, Rona
Akiva, Anat
van Wezel, Gilles P.
Kros, Alexander
Claessen, Dennis
Endocytosis-like DNA uptake by cell wall-deficient bacteria
title Endocytosis-like DNA uptake by cell wall-deficient bacteria
title_full Endocytosis-like DNA uptake by cell wall-deficient bacteria
title_fullStr Endocytosis-like DNA uptake by cell wall-deficient bacteria
title_full_unstemmed Endocytosis-like DNA uptake by cell wall-deficient bacteria
title_short Endocytosis-like DNA uptake by cell wall-deficient bacteria
title_sort endocytosis-like dna uptake by cell wall-deficient bacteria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9500057/
https://www.ncbi.nlm.nih.gov/pubmed/36138004
http://dx.doi.org/10.1038/s41467-022-33054-w
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