<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants

ABSTRACT Bacteria adopt social behavior to expand into new territory, led by specialized swarmers, before forming a biofilm. Such mass migration of Bacillus subtilis on a synthetic medium produces hyperbranching dendrites that transiently (equivalent to 4 to 5 generations of growth) maintain a cellu...

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Autores principales:	Lina Hamouche, Soumaya Laalami, Adrian Daerr, Solène Song, I. Barry Holland, Simone J. Séror, Kassem Hamze, Harald Putzer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5271839ea886466e849fbb3edf6d35d9
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spelling	oai:doaj.org-article:5271839ea886466e849fbb3edf6d35d92021-11-15T15:51:06Z<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants10.1128/mBio.02102-162150-7511https://doaj.org/article/5271839ea886466e849fbb3edf6d35d92017-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02102-16https://doaj.org/toc/2150-7511ABSTRACT Bacteria adopt social behavior to expand into new territory, led by specialized swarmers, before forming a biofilm. Such mass migration of Bacillus subtilis on a synthetic medium produces hyperbranching dendrites that transiently (equivalent to 4 to 5 generations of growth) maintain a cellular monolayer over long distances, greatly facilitating single-cell gene expression analysis. Paradoxically, while cells in the dendrites (nonswarmers) might be expected to grow exponentially, the rate of swarm expansion is constant, suggesting that some cells are not multiplying. Little attention has been paid to which cells in a swarm are actually multiplying and contributing to the overall biomass. Here, we show in situ that DNA replication, protein translation and peptidoglycan synthesis are primarily restricted to the swarmer cells at dendrite tips. Thus, these specialized cells not only lead the population forward but are apparently the source of all cells in the stems of early dendrites. We developed a simple mathematical model that supports this conclusion. IMPORTANCE Swarming motility enables rapid coordinated surface translocation of a microbial community, preceding the formation of a biofilm. This movement occurs in thin films and involves specialized swarmer cells localized to a narrow zone at the extreme swarm edge. In the B. subtilis system, using a synthetic medium, the swarm front remains as a cellular monolayer for up to 1.5 cm. Swarmers display high-velocity whirls and vortexing and are often assumed to drive community expansion at the expense of cell growth. Surprisingly, little attention has been paid to which cells in a swarm are actually growing and contributing to the overall biomass. Here, we show that swarmers not only lead the population forward but continue to multiply as a source of all cells in the community. We present a model that explains how exponential growth of only a few cells is compatible with the linear expansion rate of the swarm.Lina HamoucheSoumaya LaalamiAdrian DaerrSolène SongI. Barry HollandSimone J. SérorKassem HamzeHarald PutzerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 1 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Lina Hamouche Soumaya Laalami Adrian Daerr Solène Song I. Barry Holland Simone J. Séror Kassem Hamze Harald Putzer <italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
description	ABSTRACT Bacteria adopt social behavior to expand into new territory, led by specialized swarmers, before forming a biofilm. Such mass migration of Bacillus subtilis on a synthetic medium produces hyperbranching dendrites that transiently (equivalent to 4 to 5 generations of growth) maintain a cellular monolayer over long distances, greatly facilitating single-cell gene expression analysis. Paradoxically, while cells in the dendrites (nonswarmers) might be expected to grow exponentially, the rate of swarm expansion is constant, suggesting that some cells are not multiplying. Little attention has been paid to which cells in a swarm are actually multiplying and contributing to the overall biomass. Here, we show in situ that DNA replication, protein translation and peptidoglycan synthesis are primarily restricted to the swarmer cells at dendrite tips. Thus, these specialized cells not only lead the population forward but are apparently the source of all cells in the stems of early dendrites. We developed a simple mathematical model that supports this conclusion. IMPORTANCE Swarming motility enables rapid coordinated surface translocation of a microbial community, preceding the formation of a biofilm. This movement occurs in thin films and involves specialized swarmer cells localized to a narrow zone at the extreme swarm edge. In the B. subtilis system, using a synthetic medium, the swarm front remains as a cellular monolayer for up to 1.5 cm. Swarmers display high-velocity whirls and vortexing and are often assumed to drive community expansion at the expense of cell growth. Surprisingly, little attention has been paid to which cells in a swarm are actually growing and contributing to the overall biomass. Here, we show that swarmers not only lead the population forward but continue to multiply as a source of all cells in the community. We present a model that explains how exponential growth of only a few cells is compatible with the linear expansion rate of the swarm.
format	article
author	Lina Hamouche Soumaya Laalami Adrian Daerr Solène Song I. Barry Holland Simone J. Séror Kassem Hamze Harald Putzer
author_facet	Lina Hamouche Soumaya Laalami Adrian Daerr Solène Song I. Barry Holland Simone J. Séror Kassem Hamze Harald Putzer
author_sort	Lina Hamouche
title	<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
title_short	<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
title_full	<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
title_fullStr	<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
title_full_unstemmed	<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants
title_sort	<italic toggle="yes">bacillus subtilis</italic> swarmer cells lead the swarm, multiply, and generate a trail of quiescent descendants
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/5271839ea886466e849fbb3edf6d35d9
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<italic toggle="yes">Bacillus subtilis</italic> Swarmer Cells Lead the Swarm, Multiply, and Generate a Trail of Quiescent Descendants

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