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

Georgina Glover, Margaritis Voliotis, Urszula Łapińska, Brandon M. Invergo, Darren Soanes, Paul O’Neill, Karen Moore, Nela Nikolic, Peter G. Petrov, David S. Milner, Sumita Roy, Kate Heesom, Thomas A. Richards, Krasimira Tsaneva-Atanasova, Stefano Pagliara
doi: https://doi.org/10.1101/2022.01.26.477826
Georgina Glover
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
2Department of Physics and Astronomy, University of Exeter, Stocker Road, Exeter EX4 4QL, UK
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Margaritis Voliotis
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
3Department of Mathematics, University of Exeter, Stocker Road, Exeter, UK
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Urszula Łapińska
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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Brandon M. Invergo
5Translational Research Exchange at Exeter, University of Exeter, Exeter, United Kingdom
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Darren Soanes
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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Paul O’Neill
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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Karen Moore
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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Nela Nikolic
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
6Institute of Science and Technology Austria, 3400 Klosterneuburg, Austria
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Peter G. Petrov
2Department of Physics and Astronomy, University of Exeter, Stocker Road, Exeter EX4 4QL, UK
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David S. Milner
7Department of Zoology, University of Oxford, 11a Mansfield Road, Oxford OX1 3SZ, UK
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Sumita Roy
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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Kate Heesom
8University of Bristol Proteomics Facility, University Walk, Bristol BS8 1TD, UK
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Thomas A. Richards
7Department of Zoology, University of Oxford, 11a Mansfield Road, Oxford OX1 3SZ, UK
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Krasimira Tsaneva-Atanasova
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
3Department of Mathematics, University of Exeter, Stocker Road, Exeter, UK
9Dept. of Bioinformatics and Mathematical Modelling, Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, 105 Acad. G. Bonchev Str., 1113 Sofia, Bulgaria
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Stefano Pagliara
1Living Systems Institute, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
4Biosciences, University of Exeter, Stocker Road, Exeter EX4 4Q, UK
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  • For correspondence: S.Pagliara@exeter.ac.uk
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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. Bacterial glucose metabolism, for example, is thought to be strongly adjusted in response to cell size, yet, in contrast, the impact on glucose metabolism of multiple changes in environmental parameters is poorly understood. 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. We found that these changes in metabolic function observed 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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted January 26, 2022.
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Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
Georgina Glover, Margaritis Voliotis, Urszula Łapińska, Brandon M. Invergo, Darren Soanes, Paul O’Neill, Karen Moore, Nela Nikolic, Peter G. Petrov, David S. Milner, Sumita Roy, Kate Heesom, Thomas A. Richards, Krasimira Tsaneva-Atanasova, Stefano Pagliara
bioRxiv 2022.01.26.477826; doi: https://doi.org/10.1101/2022.01.26.477826
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Nutrient and salt depletion synergistically boosts glucose metabolism in individual Escherichia coli cells
Georgina Glover, Margaritis Voliotis, Urszula Łapińska, Brandon M. Invergo, Darren Soanes, Paul O’Neill, Karen Moore, Nela Nikolic, Peter G. Petrov, David S. Milner, Sumita Roy, Kate Heesom, Thomas A. Richards, Krasimira Tsaneva-Atanasova, Stefano Pagliara
bioRxiv 2022.01.26.477826; doi: https://doi.org/10.1101/2022.01.26.477826

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