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

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

Bacteria/metabolism, Escherichia coli/metabolism, Escherichia coli Proteins/genetics, Glucose/metabolism, Humans, Nutrients/metabolism
2399-3642
385
Glover, Georgina
6087350b-23a0-4994-ac87-e4d810a99264
Voliotis, Margaritis
78ef055d-8561-41d4-a022-6f75ecc3581f
Łapińska, Urszula
3b27d5d9-655c-4133-b996-14752b9d1008
Invergo, Brandon M
8c112b2a-67ae-4666-bb01-60548e7eff32
Soanes, Darren
6d3d8acc-8919-4eb2-a25d-1770e00a8d19
O'Neill, Paul
a6fa5954-9ada-4c94-ac42-4f5a11474bc8
Moore, Karen
92b3799c-e4a8-4af2-95c1-f70ace523032
Nikolic, Nela
88a8f576-d9e2-4eb6-9219-39b7065963d3
Petrov, Peter G
7a70e28e-f472-4389-bf68-fd28537228aa
Milner, David S
21648d2e-2b2a-4206-ade8-089fc12be305
Roy, Sumita
a9dc0438-4e8e-42c1-a5df-ef1dd3802319
Heesom, Kate
7165be53-3c8f-4b35-a139-66b8dae0af70
Richards, Thomas A
5bc939f9-1e7a-4b1c-9454-cef237a9e7b2
Tsaneva-Atanasova, Krasimira
07930ead-d534-4987-87d6-ec2b8e2ff35d
Pagliara, Stefano
b8c4e523-6190-477e-8d28-08f63dd60cf7
Glover, Georgina
6087350b-23a0-4994-ac87-e4d810a99264
Voliotis, Margaritis
78ef055d-8561-41d4-a022-6f75ecc3581f
Łapińska, Urszula
3b27d5d9-655c-4133-b996-14752b9d1008
Invergo, Brandon M
8c112b2a-67ae-4666-bb01-60548e7eff32
Soanes, Darren
6d3d8acc-8919-4eb2-a25d-1770e00a8d19
O'Neill, Paul
a6fa5954-9ada-4c94-ac42-4f5a11474bc8
Moore, Karen
92b3799c-e4a8-4af2-95c1-f70ace523032
Nikolic, Nela
88a8f576-d9e2-4eb6-9219-39b7065963d3
Petrov, Peter G
7a70e28e-f472-4389-bf68-fd28537228aa
Milner, David S
21648d2e-2b2a-4206-ade8-089fc12be305
Roy, Sumita
a9dc0438-4e8e-42c1-a5df-ef1dd3802319
Heesom, Kate
7165be53-3c8f-4b35-a139-66b8dae0af70
Richards, Thomas A
5bc939f9-1e7a-4b1c-9454-cef237a9e7b2
Tsaneva-Atanasova, Krasimira
07930ead-d534-4987-87d6-ec2b8e2ff35d
Pagliara, Stefano
b8c4e523-6190-477e-8d28-08f63dd60cf7

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 and Pagliara, Stefano (2022) Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells. Communications Biology, 5 (1), 385. (doi:10.1038/s42003-022-03336-6).

Record type: Article

Abstract

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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More information

Accepted/In Press date: 30 March 2022
Published date: 20 April 2022
Additional Information: © 2022. The Author(s).
Keywords: Bacteria/metabolism, Escherichia coli/metabolism, Escherichia coli Proteins/genetics, Glucose/metabolism, Humans, Nutrients/metabolism

Identifiers

Local EPrints ID: 488043
URI: http://eprints.soton.ac.uk/id/eprint/488043
ISSN: 2399-3642
PURE UUID: d38f0105-a739-4ea6-885d-52d44ea582fa
ORCID for Nela Nikolic: ORCID iD orcid.org/0000-0001-9068-6090

Catalogue record

Date deposited: 12 Mar 2024 18:26
Last modified: 18 Mar 2024 04:18

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Contributors

Author: Georgina Glover
Author: Margaritis Voliotis
Author: Urszula Łapińska
Author: Brandon M Invergo
Author: Darren Soanes
Author: Paul O'Neill
Author: Karen Moore
Author: Nela Nikolic ORCID iD
Author: Peter G Petrov
Author: David S Milner
Author: Sumita Roy
Author: Kate Heesom
Author: Thomas A Richards
Author: Krasimira Tsaneva-Atanasova
Author: Stefano Pagliara

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