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Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells

The interaction between a cell and its environment shapes fundamental intracellular processes such as cellular metabolism. In most cases growth rate is treated as a proximal metric for understanding the cellular metabolic status. However, changes in growth rate might not reflect metabolic variations...

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Autores principales: Glover, Georgina, Voliotis, Margaritis, Łapińska, Urszula, Invergo, Brandon M., Soanes, Darren, O’Neill, Paul, Moore, Karen, Nikolic, Nela, Petrov, Peter G., Milner, David S., Roy, Sumita, Heesom, Kate, Richards, Thomas A., Tsaneva-Atanasova, Krasimira, Pagliara, Stefano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9021252/
https://www.ncbi.nlm.nih.gov/pubmed/35444215
http://dx.doi.org/10.1038/s42003-022-03336-6
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author Glover, Georgina
Voliotis, Margaritis
Łapińska, Urszula
Invergo, Brandon M.
Soanes, Darren
O’Neill, Paul
Moore, Karen
Nikolic, Nela
Petrov, Peter G.
Milner, David S.
Roy, Sumita
Heesom, Kate
Richards, Thomas A.
Tsaneva-Atanasova, Krasimira
Pagliara, Stefano
author_facet Glover, Georgina
Voliotis, Margaritis
Łapińska, Urszula
Invergo, Brandon M.
Soanes, Darren
O’Neill, Paul
Moore, Karen
Nikolic, Nela
Petrov, Peter G.
Milner, David S.
Roy, Sumita
Heesom, Kate
Richards, Thomas A.
Tsaneva-Atanasova, Krasimira
Pagliara, Stefano
author_sort Glover, Georgina
collection PubMed
description The interaction between a cell and its environment shapes fundamental intracellular processes such as cellular metabolism. In most cases growth rate is treated as a proximal metric for understanding the cellular metabolic status. However, changes in growth rate might not reflect metabolic variations in individuals responding to environmental fluctuations. Here we use single-cell microfluidics-microscopy combined with transcriptomics, proteomics and mathematical modelling to quantify the accumulation of glucose within Escherichia coli cells. In contrast to the current consensus, we reveal that environmental conditions which are comparatively unfavourable for growth, where both nutrients and salinity are depleted, increase glucose accumulation rates in individual bacteria and population subsets. We find that these changes in metabolic function are underpinned by variations at the translational and posttranslational level but not at the transcriptional level and are not dictated by changes in cell size. The metabolic response-characteristics identified greatly advance our fundamental understanding of the interactions between bacteria and their environment and have important ramifications when investigating cellular processes where salinity plays an important role.
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spelling pubmed-90212522022-04-28 Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells Glover, Georgina Voliotis, Margaritis Łapińska, Urszula Invergo, Brandon M. Soanes, Darren O’Neill, Paul Moore, Karen Nikolic, Nela Petrov, Peter G. Milner, David S. Roy, Sumita Heesom, Kate Richards, Thomas A. Tsaneva-Atanasova, Krasimira Pagliara, Stefano Commun Biol Article The interaction between a cell and its environment shapes fundamental intracellular processes such as cellular metabolism. In most cases growth rate is treated as a proximal metric for understanding the cellular metabolic status. However, changes in growth rate might not reflect metabolic variations in individuals responding to environmental fluctuations. Here we use single-cell microfluidics-microscopy combined with transcriptomics, proteomics and mathematical modelling to quantify the accumulation of glucose within Escherichia coli cells. In contrast to the current consensus, we reveal that environmental conditions which are comparatively unfavourable for growth, where both nutrients and salinity are depleted, increase glucose accumulation rates in individual bacteria and population subsets. We find that these changes in metabolic function are underpinned by variations at the translational and posttranslational level but not at the transcriptional level and are not dictated by changes in cell size. The metabolic response-characteristics identified greatly advance our fundamental understanding of the interactions between bacteria and their environment and have important ramifications when investigating cellular processes where salinity plays an important role. Nature Publishing Group UK 2022-04-20 /pmc/articles/PMC9021252/ /pubmed/35444215 http://dx.doi.org/10.1038/s42003-022-03336-6 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Glover, Georgina
Voliotis, Margaritis
Łapińska, Urszula
Invergo, Brandon M.
Soanes, Darren
O’Neill, Paul
Moore, Karen
Nikolic, Nela
Petrov, Peter G.
Milner, David S.
Roy, Sumita
Heesom, Kate
Richards, Thomas A.
Tsaneva-Atanasova, Krasimira
Pagliara, Stefano
Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title_full Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title_fullStr Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title_full_unstemmed Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title_short Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
title_sort nutrient and salt depletion synergistically boosts glucose metabolism in individual escherichia coli cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9021252/
https://www.ncbi.nlm.nih.gov/pubmed/35444215
http://dx.doi.org/10.1038/s42003-022-03336-6
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