Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>

ABSTRACT Dividing cells of the coccoid Gram-positive bacterium Staphylococcus aureus undergo extremely rapid (millisecond) daughter cell separation (DCS) driven by mechanical crack propagation, a strategy that is very distinct from the gradual, enzymatically driven cell wall remodeling process that...

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Autores principales: Xiaoxue Zhou, David K. Halladin, Julie A. Theriot
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:3a72ad9217b54c6f896b313e260e07cb2021-11-15T15:50:19ZFast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>10.1128/mBio.00952-162150-7511https://doaj.org/article/3a72ad9217b54c6f896b313e260e07cb2016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00952-16https://doaj.org/toc/2150-7511ABSTRACT Dividing cells of the coccoid Gram-positive bacterium Staphylococcus aureus undergo extremely rapid (millisecond) daughter cell separation (DCS) driven by mechanical crack propagation, a strategy that is very distinct from the gradual, enzymatically driven cell wall remodeling process that has been well described in several rod-shaped model bacteria. To determine if other bacteria, especially those in the same phylum (Firmicutes) or with similar coccoid shapes as S. aureus, might use a similar mechanically driven strategy for DCS, we used high-resolution video microscopy to examine cytokinesis in a phylogenetically wide range of species with various cell shapes and sizes. We found that fast mechanically driven DCS is rather rare in the Firmicutes (low G+C Gram positives), observed only in Staphylococcus and its closest coccoid relatives in the Macrococcus genus, and we did not observe this division strategy among the Gram-negative Proteobacteria. In contrast, several members of the high-G+C Gram-positive phylum Actinobacteria (Micrococcus luteus, Brachybacterium faecium, Corynebacterium glutamicum, and Mycobacterium smegmatis) with diverse shapes ranging from coccoid to rod all undergo fast mechanical DCS during cell division. Most intriguingly, similar fast mechanical DCS was also observed during the sporulation of the actinobacterium Streptomyces venezuelae. IMPORTANCE Much of our knowledge on bacterial cytokinesis comes from studying rod-shaped model organisms such as Escherichia coli and Bacillus subtilis. Less is known about variations in this process among different bacterial species. While cell division in many bacteria has been characterized to some extent genetically or biochemically, few species have been examined using video microscopy to uncover the kinetics of cytokinesis and daughter cell separation (DCS). In this work, we found that fast (millisecond) DCS is exhibited by species in two independent clades of Gram-positive bacteria and is particularly prevalent among the Actinobacteria, a diverse group that includes significant pathogens as well as bacteria that generate medically important antibiotics.Xiaoxue ZhouDavid K. HalladinJulie A. TheriotAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Xiaoxue Zhou
David K. Halladin
Julie A. Theriot
Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
description ABSTRACT Dividing cells of the coccoid Gram-positive bacterium Staphylococcus aureus undergo extremely rapid (millisecond) daughter cell separation (DCS) driven by mechanical crack propagation, a strategy that is very distinct from the gradual, enzymatically driven cell wall remodeling process that has been well described in several rod-shaped model bacteria. To determine if other bacteria, especially those in the same phylum (Firmicutes) or with similar coccoid shapes as S. aureus, might use a similar mechanically driven strategy for DCS, we used high-resolution video microscopy to examine cytokinesis in a phylogenetically wide range of species with various cell shapes and sizes. We found that fast mechanically driven DCS is rather rare in the Firmicutes (low G+C Gram positives), observed only in Staphylococcus and its closest coccoid relatives in the Macrococcus genus, and we did not observe this division strategy among the Gram-negative Proteobacteria. In contrast, several members of the high-G+C Gram-positive phylum Actinobacteria (Micrococcus luteus, Brachybacterium faecium, Corynebacterium glutamicum, and Mycobacterium smegmatis) with diverse shapes ranging from coccoid to rod all undergo fast mechanical DCS during cell division. Most intriguingly, similar fast mechanical DCS was also observed during the sporulation of the actinobacterium Streptomyces venezuelae. IMPORTANCE Much of our knowledge on bacterial cytokinesis comes from studying rod-shaped model organisms such as Escherichia coli and Bacillus subtilis. Less is known about variations in this process among different bacterial species. While cell division in many bacteria has been characterized to some extent genetically or biochemically, few species have been examined using video microscopy to uncover the kinetics of cytokinesis and daughter cell separation (DCS). In this work, we found that fast (millisecond) DCS is exhibited by species in two independent clades of Gram-positive bacteria and is particularly prevalent among the Actinobacteria, a diverse group that includes significant pathogens as well as bacteria that generate medically important antibiotics.
format article
author Xiaoxue Zhou
David K. Halladin
Julie A. Theriot
author_facet Xiaoxue Zhou
David K. Halladin
Julie A. Theriot
author_sort Xiaoxue Zhou
title Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
title_short Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
title_full Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
title_fullStr Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
title_full_unstemmed Fast Mechanically Driven Daughter Cell Separation Is Widespread in <italic toggle="yes">Actinobacteria</italic>
title_sort fast mechanically driven daughter cell separation is widespread in <italic toggle="yes">actinobacteria</italic>
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/3a72ad9217b54c6f896b313e260e07cb
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AT julieatheriot fastmechanicallydrivendaughtercellseparationiswidespreadinitalictoggleyesactinobacteriaitalic
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