The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae

Autores
Thoke, Henrik S.; Thorsteinsson, Sigmundur; Stock, Roberto P.; Bagatolli, Luis Alberto; Olsen, Lars F.
Año de publicación
2017
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
We explored the dynamic coupling of intracellular water with metabolism in yeast cells. Using the polarity-sensitive probe 6-acetyl-2-dimethylaminonaphthalene (ACDAN), we show that glycolytic oscillations in the yeast S. cerevisiae BY4743 wild-type strain are coupled to the generalized polarization (GP) function of ACDAN, which measures the physical state of intracellular water. We analysed the oscillatory dynamics in wild type and 24 mutant strains with mutations in many different enzymes and proteins. Using fluorescence spectroscopy, we measured the amplitude and frequency of the metabolic oscillations and ACDAN GP in the resting state of all 25 strains. The results showed that there is a lower and an upper threshold of ACDAN GP, beyond which oscillations do not occur. This critical GP range is also phenomenologically linked to the occurrence of oscillations when cells are grown at different temperatures. Furthermore, the link between glycolytic oscillations and the ACDAN GP value also holds when ATP synthesis or the integrity of the cell cytoskeleton is perturbed. Our results represent the first demonstration that the dynamic behaviour of a metabolic process can be regulated by a cell-wide physical property: the dynamic state of intracellular water, which represents an emergent property.
Fil: Thoke, Henrik S.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; Dinamarca
Fil: Thorsteinsson, Sigmundur. University of Southern Denmark; Dinamarca
Fil: Stock, Roberto P.. University of Southern Denmark; Dinamarca
Fil: Bagatolli, Luis Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Center for Biomembrane Physics; Dinamarca. Yachay EP and Yachay Tech; Ecuador
Fil: Olsen, Lars F.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; Dinamarca
Materia
Intracelullar water dynamics
Acdan
Glycolytic oscillations
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/63941
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/63941
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network_name_str CONICET Digital (CONICET)
spelling The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiaeThoke, Henrik S.Thorsteinsson, SigmundurStock, Roberto P.Bagatolli, Luis AlbertoOlsen, Lars F.Intracelullar water dynamicsAcdanGlycolytic oscillationshttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1We explored the dynamic coupling of intracellular water with metabolism in yeast cells. Using the polarity-sensitive probe 6-acetyl-2-dimethylaminonaphthalene (ACDAN), we show that glycolytic oscillations in the yeast S. cerevisiae BY4743 wild-type strain are coupled to the generalized polarization (GP) function of ACDAN, which measures the physical state of intracellular water. We analysed the oscillatory dynamics in wild type and 24 mutant strains with mutations in many different enzymes and proteins. Using fluorescence spectroscopy, we measured the amplitude and frequency of the metabolic oscillations and ACDAN GP in the resting state of all 25 strains. The results showed that there is a lower and an upper threshold of ACDAN GP, beyond which oscillations do not occur. This critical GP range is also phenomenologically linked to the occurrence of oscillations when cells are grown at different temperatures. Furthermore, the link between glycolytic oscillations and the ACDAN GP value also holds when ATP synthesis or the integrity of the cell cytoskeleton is perturbed. Our results represent the first demonstration that the dynamic behaviour of a metabolic process can be regulated by a cell-wide physical property: the dynamic state of intracellular water, which represents an emergent property.Fil: Thoke, Henrik S.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; DinamarcaFil: Thorsteinsson, Sigmundur. University of Southern Denmark; DinamarcaFil: Stock, Roberto P.. University of Southern Denmark; DinamarcaFil: Bagatolli, Luis Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Center for Biomembrane Physics; Dinamarca. Yachay EP and Yachay Tech; EcuadorFil: Olsen, Lars F.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; DinamarcaNature Publishing Group2017-12-24info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/63941Thoke, Henrik S.; Thorsteinsson, Sigmundur; Stock, Roberto P.; Bagatolli, Luis Alberto; Olsen, Lars F.; The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae; Nature Publishing Group; Scientific Reports; 7; 1; 24-12-2017; 162502045-2322CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-017-16442-xinfo:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41598-017-16442-xinfo:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:45:53Zoai:ri.conicet.gov.ar:11336/63941instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:45:53.859CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
title The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
spellingShingle The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
Thoke, Henrik S.
Intracelullar water dynamics
Acdan
Glycolytic oscillations
title_short The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
title_full The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
title_fullStr The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
title_full_unstemmed The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
title_sort The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae
dc.creator.none.fl_str_mv Thoke, Henrik S.
Thorsteinsson, Sigmundur
Stock, Roberto P.
Bagatolli, Luis Alberto
Olsen, Lars F.
author Thoke, Henrik S.
author_facet Thoke, Henrik S.
Thorsteinsson, Sigmundur
Stock, Roberto P.
Bagatolli, Luis Alberto
Olsen, Lars F.
author_role author
author2 Thorsteinsson, Sigmundur
Stock, Roberto P.
Bagatolli, Luis Alberto
Olsen, Lars F.
author2_role author
author
author
author
dc.subject.none.fl_str_mv Intracelullar water dynamics
Acdan
Glycolytic oscillations
topic Intracelullar water dynamics
Acdan
Glycolytic oscillations
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv We explored the dynamic coupling of intracellular water with metabolism in yeast cells. Using the polarity-sensitive probe 6-acetyl-2-dimethylaminonaphthalene (ACDAN), we show that glycolytic oscillations in the yeast S. cerevisiae BY4743 wild-type strain are coupled to the generalized polarization (GP) function of ACDAN, which measures the physical state of intracellular water. We analysed the oscillatory dynamics in wild type and 24 mutant strains with mutations in many different enzymes and proteins. Using fluorescence spectroscopy, we measured the amplitude and frequency of the metabolic oscillations and ACDAN GP in the resting state of all 25 strains. The results showed that there is a lower and an upper threshold of ACDAN GP, beyond which oscillations do not occur. This critical GP range is also phenomenologically linked to the occurrence of oscillations when cells are grown at different temperatures. Furthermore, the link between glycolytic oscillations and the ACDAN GP value also holds when ATP synthesis or the integrity of the cell cytoskeleton is perturbed. Our results represent the first demonstration that the dynamic behaviour of a metabolic process can be regulated by a cell-wide physical property: the dynamic state of intracellular water, which represents an emergent property.
Fil: Thoke, Henrik S.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; Dinamarca
Fil: Thorsteinsson, Sigmundur. University of Southern Denmark; Dinamarca
Fil: Stock, Roberto P.. University of Southern Denmark; Dinamarca
Fil: Bagatolli, Luis Alberto. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Center for Biomembrane Physics; Dinamarca. Yachay EP and Yachay Tech; Ecuador
Fil: Olsen, Lars F.. Center for Biomembrane Physics; Dinamarca. University of Southern Denmark; Dinamarca
description We explored the dynamic coupling of intracellular water with metabolism in yeast cells. Using the polarity-sensitive probe 6-acetyl-2-dimethylaminonaphthalene (ACDAN), we show that glycolytic oscillations in the yeast S. cerevisiae BY4743 wild-type strain are coupled to the generalized polarization (GP) function of ACDAN, which measures the physical state of intracellular water. We analysed the oscillatory dynamics in wild type and 24 mutant strains with mutations in many different enzymes and proteins. Using fluorescence spectroscopy, we measured the amplitude and frequency of the metabolic oscillations and ACDAN GP in the resting state of all 25 strains. The results showed that there is a lower and an upper threshold of ACDAN GP, beyond which oscillations do not occur. This critical GP range is also phenomenologically linked to the occurrence of oscillations when cells are grown at different temperatures. Furthermore, the link between glycolytic oscillations and the ACDAN GP value also holds when ATP synthesis or the integrity of the cell cytoskeleton is perturbed. Our results represent the first demonstration that the dynamic behaviour of a metabolic process can be regulated by a cell-wide physical property: the dynamic state of intracellular water, which represents an emergent property.
publishDate 2017
dc.date.none.fl_str_mv 2017-12-24
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/63941
Thoke, Henrik S.; Thorsteinsson, Sigmundur; Stock, Roberto P.; Bagatolli, Luis Alberto; Olsen, Lars F.; The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae; Nature Publishing Group; Scientific Reports; 7; 1; 24-12-2017; 16250
2045-2322
CONICET Digital
CONICET
url http://hdl.handle.net/11336/63941
identifier_str_mv Thoke, Henrik S.; Thorsteinsson, Sigmundur; Stock, Roberto P.; Bagatolli, Luis Alberto; Olsen, Lars F.; The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae; Nature Publishing Group; Scientific Reports; 7; 1; 24-12-2017; 16250
2045-2322
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-017-16442-x
info:eu-repo/semantics/altIdentifier/url/https://www.nature.com/articles/s41598-017-16442-x
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Nature Publishing Group
publisher.none.fl_str_mv Nature Publishing Group
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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