<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming

ABSTRACT Many flagellated bacteria “swarm” over a solid surface as a dense consortium. In different bacteria, swarming is facilitated by several alterations such as those corresponding to increased flagellum numbers, special stator proteins, or secreted surfactants. We report here a change in the ch...

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Autores principales:	Jonathan D. Partridge, Nguyen T. Q. Nhu, Yann S. Dufour, Rasika M. Harshey
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	CheZ chemotaxis flagellar motility Lévy walk swarming Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4dd46dbfc93d44d698d65ef2a9a202f4
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spelling	oai:doaj.org-article:4dd46dbfc93d44d698d65ef2a9a202f42021-11-15T15:55:25Z<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming10.1128/mBio.00316-192150-7511https://doaj.org/article/4dd46dbfc93d44d698d65ef2a9a202f42019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00316-19https://doaj.org/toc/2150-7511ABSTRACT Many flagellated bacteria “swarm” over a solid surface as a dense consortium. In different bacteria, swarming is facilitated by several alterations such as those corresponding to increased flagellum numbers, special stator proteins, or secreted surfactants. We report here a change in the chemosensory physiology of swarming Escherichia coli which alters its normal “run tumble” bias. E. coli bacteria taken from a swarm exhibit more highly extended runs (low tumble bias) and higher speeds than E. coli bacteria swimming individually in a liquid medium. The stability of the signaling protein CheZ is higher in swarmers, consistent with the observed elevation of CheZ levels and with the low tumble bias. We show that the tumble bias displayed by wild-type swarmers is the optimal bias for maximizing swarm expansion. In assays performed in liquid, swarm cells have reduced chemotactic performance. This behavior is specific to swarming, is not specific to growth on surfaces, and persists for a generation. Therefore, the chemotaxis signaling pathway is reprogrammed for swarming. IMPORTANCE The fundamental motile behavior of E. coli is a random walk, where straight “runs” are punctuated by “tumbles.” This behavior, conferred by the chemotaxis signaling system, is used to track chemical gradients in liquid. Our study results show that when migrating collectively on surfaces, E. coli modifies its chemosensory physiology to decrease its tumble bias (and hence to increase run durations) by post-transcriptional changes that alter the levels of a key signaling protein. We speculate that the low tumble bias may contribute to the observed Lévy walk (LW) trajectories within the swarm, where run durations have a power law distribution. In animals, LW patterns are hypothesized to maximize searches in unpredictable environments. Swarming bacteria face several challenges while moving collectively over a surface—maintaining cohesion, overcoming constraints imposed by a physical substrate, searching for nutrients as a group, and surviving lethal levels of antimicrobials. The altered chemosensory behavior that we describe in this report may help with these challenges.Jonathan D. PartridgeNguyen T. Q. NhuYann S. DufourRasika M. HarsheyAmerican Society for MicrobiologyarticleCheZchemotaxisflagellar motilityLévy walkswarmingMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	CheZ chemotaxis flagellar motility Lévy walk swarming Microbiology QR1-502
spellingShingle	CheZ chemotaxis flagellar motility Lévy walk swarming Microbiology QR1-502 Jonathan D. Partridge Nguyen T. Q. Nhu Yann S. Dufour Rasika M. Harshey <italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
description	ABSTRACT Many flagellated bacteria “swarm” over a solid surface as a dense consortium. In different bacteria, swarming is facilitated by several alterations such as those corresponding to increased flagellum numbers, special stator proteins, or secreted surfactants. We report here a change in the chemosensory physiology of swarming Escherichia coli which alters its normal “run tumble” bias. E. coli bacteria taken from a swarm exhibit more highly extended runs (low tumble bias) and higher speeds than E. coli bacteria swimming individually in a liquid medium. The stability of the signaling protein CheZ is higher in swarmers, consistent with the observed elevation of CheZ levels and with the low tumble bias. We show that the tumble bias displayed by wild-type swarmers is the optimal bias for maximizing swarm expansion. In assays performed in liquid, swarm cells have reduced chemotactic performance. This behavior is specific to swarming, is not specific to growth on surfaces, and persists for a generation. Therefore, the chemotaxis signaling pathway is reprogrammed for swarming. IMPORTANCE The fundamental motile behavior of E. coli is a random walk, where straight “runs” are punctuated by “tumbles.” This behavior, conferred by the chemotaxis signaling system, is used to track chemical gradients in liquid. Our study results show that when migrating collectively on surfaces, E. coli modifies its chemosensory physiology to decrease its tumble bias (and hence to increase run durations) by post-transcriptional changes that alter the levels of a key signaling protein. We speculate that the low tumble bias may contribute to the observed Lévy walk (LW) trajectories within the swarm, where run durations have a power law distribution. In animals, LW patterns are hypothesized to maximize searches in unpredictable environments. Swarming bacteria face several challenges while moving collectively over a surface—maintaining cohesion, overcoming constraints imposed by a physical substrate, searching for nutrients as a group, and surviving lethal levels of antimicrobials. The altered chemosensory behavior that we describe in this report may help with these challenges.
format	article
author	Jonathan D. Partridge Nguyen T. Q. Nhu Yann S. Dufour Rasika M. Harshey
author_facet	Jonathan D. Partridge Nguyen T. Q. Nhu Yann S. Dufour Rasika M. Harshey
author_sort	Jonathan D. Partridge
title	<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
title_short	<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
title_full	<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
title_fullStr	<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
title_full_unstemmed	<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming
title_sort	<italic toggle="yes">escherichia coli</italic> remodels the chemotaxis pathway for swarming
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/4dd46dbfc93d44d698d65ef2a9a202f4
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<italic toggle="yes">Escherichia coli</italic> Remodels the Chemotaxis Pathway for Swarming

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