A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium

ABSTRACT Many bacteria are motile only when nutrients are scarce. In contrast, Salmonella enterica serovar Typhimurium is motile only when nutrients are plentiful, suggesting that this bacterium uses motility for purposes other than foraging, most likely for host colonization. In this study, we inve...

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Autores principales: Santosh Koirala, Patrick Mears, Martin Sim, Ido Golding, Yann R. Chemla, Phillip D. Aldridge, Christopher V. Rao
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:bfddc0d189cf45088d25a0d28907bfa22021-11-15T15:45:54ZA Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium10.1128/mBio.01611-142150-7511https://doaj.org/article/bfddc0d189cf45088d25a0d28907bfa22014-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01611-14https://doaj.org/toc/2150-7511ABSTRACT Many bacteria are motile only when nutrients are scarce. In contrast, Salmonella enterica serovar Typhimurium is motile only when nutrients are plentiful, suggesting that this bacterium uses motility for purposes other than foraging, most likely for host colonization. In this study, we investigated how nutrients affect motility in S. enterica and found that they tune the fraction of motile cells. In particular, we observed coexisting populations of motile and nonmotile cells, with the distribution being determined by the concentration of nutrients in the growth medium. Interestingly, S. enterica responds not to a single nutrient but apparently to a complex mixture of them. Using a combination of experimentation and mathematical modeling, we investigated the mechanism governing this behavior and found that it results from two antagonizing regulatory proteins, FliZ and YdiV. We also found that a positive feedback loop involving the alternate sigma factor FliA is required, although its role appears solely to amplify FliZ expression. We further demonstrate that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. Together, these results uncover a new facet of the regulation of the flagellar genes in S. enterica and further demonstrate how bacteria employ phenotypic diversity as a general mechanism for adapting to change in their environment. IMPORTANCE Many bacteria employ flagella for motility. These bacteria are often not constitutively motile but become so only in response to specific environmental cues. The most common is nutrient starvation. Interestingly, in Salmonella enterica serovar Typhimurium, nutrients enhance the expression of flagella, suggesting that motility is used for purposes other than foraging. In this work, we investigated how nutrients affect motility in S. enterica and found that nutrients tune the fraction of motile cells within a population. Using both experimental and mathematical analysis, we determined the mechanism governing this tunable response. We further demonstrated that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. These results reveal a new facet of motility in S. enterica and demonstrate that nutrients determine not only where these bacteria swim but also the fraction of them that do so.Santosh KoiralaPatrick MearsMartin SimIdo GoldingYann R. ChemlaPhillip D. AldridgeChristopher V. RaoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 5 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Santosh Koirala
Patrick Mears
Martin Sim
Ido Golding
Yann R. Chemla
Phillip D. Aldridge
Christopher V. Rao
A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
description ABSTRACT Many bacteria are motile only when nutrients are scarce. In contrast, Salmonella enterica serovar Typhimurium is motile only when nutrients are plentiful, suggesting that this bacterium uses motility for purposes other than foraging, most likely for host colonization. In this study, we investigated how nutrients affect motility in S. enterica and found that they tune the fraction of motile cells. In particular, we observed coexisting populations of motile and nonmotile cells, with the distribution being determined by the concentration of nutrients in the growth medium. Interestingly, S. enterica responds not to a single nutrient but apparently to a complex mixture of them. Using a combination of experimentation and mathematical modeling, we investigated the mechanism governing this behavior and found that it results from two antagonizing regulatory proteins, FliZ and YdiV. We also found that a positive feedback loop involving the alternate sigma factor FliA is required, although its role appears solely to amplify FliZ expression. We further demonstrate that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. Together, these results uncover a new facet of the regulation of the flagellar genes in S. enterica and further demonstrate how bacteria employ phenotypic diversity as a general mechanism for adapting to change in their environment. IMPORTANCE Many bacteria employ flagella for motility. These bacteria are often not constitutively motile but become so only in response to specific environmental cues. The most common is nutrient starvation. Interestingly, in Salmonella enterica serovar Typhimurium, nutrients enhance the expression of flagella, suggesting that motility is used for purposes other than foraging. In this work, we investigated how nutrients affect motility in S. enterica and found that nutrients tune the fraction of motile cells within a population. Using both experimental and mathematical analysis, we determined the mechanism governing this tunable response. We further demonstrated that the response is bistable: that is, genetically identical cells can exhibit different phenotypes under identical growth conditions. These results reveal a new facet of motility in S. enterica and demonstrate that nutrients determine not only where these bacteria swim but also the fraction of them that do so.
format article
author Santosh Koirala
Patrick Mears
Martin Sim
Ido Golding
Yann R. Chemla
Phillip D. Aldridge
Christopher V. Rao
author_facet Santosh Koirala
Patrick Mears
Martin Sim
Ido Golding
Yann R. Chemla
Phillip D. Aldridge
Christopher V. Rao
author_sort Santosh Koirala
title A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
title_short A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
title_full A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
title_fullStr A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
title_full_unstemmed A Nutrient-Tunable Bistable Switch Controls Motility in <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhimurium
title_sort nutrient-tunable bistable switch controls motility in <named-content content-type="genus-species">salmonella enterica</named-content> serovar typhimurium
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/bfddc0d189cf45088d25a0d28907bfa2
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