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Sulfur sequestration promotes multicellularity during nutrient limitation

The behaviour of Dictyostelium discoideum depends on nutrients(1). When sufficient food is present these amoebae exist in a unicellular state, but upon starvation they aggregate into a multicellular organism(2,3). This biology makes D. discoideum an ideal model for investigating how fundamental meta...

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Autores principales: Kelly, Beth, Carrizo, Gustavo E., Edwards-Hicks, Joy, Sanin, David E., Stanczak, Michal A., Priesnitz, Chantal, Flachsmann, Lea J., Curtis, Jonathan D., Mittler, Gerhard, Musa, Yaarub, Becker, Thomas, Buescher, Joerg M., Pearce, Erika L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7969356/
https://www.ncbi.nlm.nih.gov/pubmed/33627869
http://dx.doi.org/10.1038/s41586-021-03270-3
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author Kelly, Beth
Carrizo, Gustavo E.
Edwards-Hicks, Joy
Sanin, David E.
Stanczak, Michal A.
Priesnitz, Chantal
Flachsmann, Lea J.
Curtis, Jonathan D.
Mittler, Gerhard
Musa, Yaarub
Becker, Thomas
Buescher, Joerg M.
Pearce, Erika L.
author_facet Kelly, Beth
Carrizo, Gustavo E.
Edwards-Hicks, Joy
Sanin, David E.
Stanczak, Michal A.
Priesnitz, Chantal
Flachsmann, Lea J.
Curtis, Jonathan D.
Mittler, Gerhard
Musa, Yaarub
Becker, Thomas
Buescher, Joerg M.
Pearce, Erika L.
author_sort Kelly, Beth
collection PubMed
description The behaviour of Dictyostelium discoideum depends on nutrients(1). When sufficient food is present these amoebae exist in a unicellular state, but upon starvation they aggregate into a multicellular organism(2,3). This biology makes D. discoideum an ideal model for investigating how fundamental metabolism commands cell differentiation and function. Here we show that reactive oxygen species—generated as a consequence of nutrient limitation—lead to the sequestration of cysteine in the antioxidant glutathione. This sequestration limits the use of the sulfur atom of cysteine in processes that contribute to mitochondrial metabolism and cellular proliferation, such as protein translation and the activity of enzymes that contain an iron–sulfur cluster. The regulated sequestration of sulfur maintains D. discoideum in a nonproliferating state that paves the way for multicellular development. This mechanism of signalling through reactive oxygen species highlights oxygen and sulfur as simple signalling molecules that dictate cell fate in an early eukaryote, with implications for responses to nutrient fluctuations in multicellular eukaryotes.
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spelling pubmed-79693562021-03-28 Sulfur sequestration promotes multicellularity during nutrient limitation Kelly, Beth Carrizo, Gustavo E. Edwards-Hicks, Joy Sanin, David E. Stanczak, Michal A. Priesnitz, Chantal Flachsmann, Lea J. Curtis, Jonathan D. Mittler, Gerhard Musa, Yaarub Becker, Thomas Buescher, Joerg M. Pearce, Erika L. Nature Article The behaviour of Dictyostelium discoideum depends on nutrients(1). When sufficient food is present these amoebae exist in a unicellular state, but upon starvation they aggregate into a multicellular organism(2,3). This biology makes D. discoideum an ideal model for investigating how fundamental metabolism commands cell differentiation and function. Here we show that reactive oxygen species—generated as a consequence of nutrient limitation—lead to the sequestration of cysteine in the antioxidant glutathione. This sequestration limits the use of the sulfur atom of cysteine in processes that contribute to mitochondrial metabolism and cellular proliferation, such as protein translation and the activity of enzymes that contain an iron–sulfur cluster. The regulated sequestration of sulfur maintains D. discoideum in a nonproliferating state that paves the way for multicellular development. This mechanism of signalling through reactive oxygen species highlights oxygen and sulfur as simple signalling molecules that dictate cell fate in an early eukaryote, with implications for responses to nutrient fluctuations in multicellular eukaryotes. Nature Publishing Group UK 2021-02-24 2021 /pmc/articles/PMC7969356/ /pubmed/33627869 http://dx.doi.org/10.1038/s41586-021-03270-3 Text en © The Author(s) 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Kelly, Beth
Carrizo, Gustavo E.
Edwards-Hicks, Joy
Sanin, David E.
Stanczak, Michal A.
Priesnitz, Chantal
Flachsmann, Lea J.
Curtis, Jonathan D.
Mittler, Gerhard
Musa, Yaarub
Becker, Thomas
Buescher, Joerg M.
Pearce, Erika L.
Sulfur sequestration promotes multicellularity during nutrient limitation
title Sulfur sequestration promotes multicellularity during nutrient limitation
title_full Sulfur sequestration promotes multicellularity during nutrient limitation
title_fullStr Sulfur sequestration promotes multicellularity during nutrient limitation
title_full_unstemmed Sulfur sequestration promotes multicellularity during nutrient limitation
title_short Sulfur sequestration promotes multicellularity during nutrient limitation
title_sort sulfur sequestration promotes multicellularity during nutrient limitation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7969356/
https://www.ncbi.nlm.nih.gov/pubmed/33627869
http://dx.doi.org/10.1038/s41586-021-03270-3
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