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The energy requirements of ion homeostasis determine the lifespan of starving bacteria

View ORCID ProfileSeverin Schink, View ORCID ProfileMark Polk, Edward Athaide, View ORCID ProfileAvik Mukherjee, Constantin Ammar, Xili Liu, View ORCID ProfileSeungeun Oh, Yu-Fang Chang, Markus Basan
doi: https://doi.org/10.1101/2021.11.22.469587
Severin Schink
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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  • For correspondence: severin_schink@hms.harvard.edu markus@hms.harvard.edu
Mark Polk
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Edward Athaide
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Avik Mukherjee
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Constantin Ammar
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
2Department of Informatics, Ludwig-Maximilians-Universität München, Amalienstrasse 17, 80333 München, Germany
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Xili Liu
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Seungeun Oh
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Yu-Fang Chang
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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Markus Basan
1Systems Biology Department, Harvard Medical School, 200 Longwood Ave, 02115 MA, USA
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  • For correspondence: severin_schink@hms.harvard.edu markus@hms.harvard.edu
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Abstract

The majority of microbes on earth, whether they live in the ocean, the soil or in animals, are not growing, but instead struggling to survive starvation. Some genes and environmental conditions affecting starvation survival have been identified, but despite almost a century of study, we do not know which processes lead to irreversible loss of viability, which maintenance processes counteract them and how lifespan is determined from the balance of these opposing processes. Here, we used time-lapse microscopy to capture and characterize the cell death process of E. coli during carbon starvation for the first time. We found that a lack of nutrients results in the collapse of ion homeostasis, triggering a positive-feedback cascade of osmotic swelling and membrane permeabilization that ultimately results in lysis. Based on these findings, we hypothesized that ion transport is the major energetic requirement for starving cells and the primary determinant of the timing of lysis. We therefore developed a mathematical model that integrates ion homeostasis and cannibalistic nutrient recycling from perished cells to predict lifespan changes under diverse conditions, such as changes of cell size, medium composition, and prior growth conditions. Guided by model predictions, we found that cell death during starvation could be dramatically slowed by replacing inorganic ions from the medium with a non-permeating osmoprotectant, removing the cost of ion homeostasis and preventing lysis. Our quantitative and predictive model explains how survival kinetics are determined in starvation and elucidates the mechanistic underpinnings of starvation survival.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • In the revised version we specified the funding source that supported XL and SO.

Copyright 
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-NC-ND 4.0 International license.
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Posted June 16, 2022.
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The energy requirements of ion homeostasis determine the lifespan of starving bacteria
Severin Schink, Mark Polk, Edward Athaide, Avik Mukherjee, Constantin Ammar, Xili Liu, Seungeun Oh, Yu-Fang Chang, Markus Basan
bioRxiv 2021.11.22.469587; doi: https://doi.org/10.1101/2021.11.22.469587
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The energy requirements of ion homeostasis determine the lifespan of starving bacteria
Severin Schink, Mark Polk, Edward Athaide, Avik Mukherjee, Constantin Ammar, Xili Liu, Seungeun Oh, Yu-Fang Chang, Markus Basan
bioRxiv 2021.11.22.469587; doi: https://doi.org/10.1101/2021.11.22.469587

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