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A conserved pressure-driven mechanism for regulating cytosolic osmolarity

View ORCID ProfileKatrina B. Velle, View ORCID ProfileRikki M. Garner, Tatihana K. Beckford, Makaela Weeda, View ORCID ProfileChunzi Liu, View ORCID ProfileAndrew S. Kennard, Marc Edwards, View ORCID ProfileLillian K. Fritz-Laylin
doi: https://doi.org/10.1101/2023.03.01.529730
Katrina B. Velle
1Department of Biology, University of Massachusetts Amherst, Amherst, MA
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Rikki M. Garner
2Department of Systems Biology, Harvard Medical School, Boston, MA
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Tatihana K. Beckford
1Department of Biology, University of Massachusetts Amherst, Amherst, MA
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Makaela Weeda
3Department of Biology, Amherst College, Amherst, MA
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Chunzi Liu
4Department of Applied Mathematics, Harvard University, Cambridge, MA
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Andrew S. Kennard
1Department of Biology, University of Massachusetts Amherst, Amherst, MA
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Marc Edwards
3Department of Biology, Amherst College, Amherst, MA
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Lillian K. Fritz-Laylin
1Department of Biology, University of Massachusetts Amherst, Amherst, MA
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  • For correspondence: lfritzlaylin@umass.edu
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ABSTRACT

Controlling intracellular osmolarity is essential to all cellular life. Cells that live in hypo-osmotic environments like freshwater must constantly battle water influx to avoid swelling until they burst. Many eukaryotic cells use contractile vacuoles to collect excess water from the cytosol and pump it out of the cell. Although contractile vacuoles are essential to many species, including important pathogens, the mechanisms that control their dynamics remain unclear. To identify basic principles governing contractile vacuole function, we here investigate the molecular mechanisms of two species with distinct vacuolar morphologies from different eukaryotic lineages—the discoban Naegleria gruberi, and the amoebozoan slime mold Dictyostelium discoideum. Using quantitative cell biology we find that, although these species respond differently to osmotic challenges, they both use actin for osmoregulation, as well as vacuolar-type proton pumps for filling contractile vacuoles. We also use analytical modeling to show that cytoplasmic pressure is sufficient to drive water out of contractile vacuoles in these species, similar to findings from the alveolate Paramecium multimicronucleatum. Because these three lineages diverged well over a billion years ago, we propose that this represents an ancient eukaryotic mechanism of osmoregulation.

Competing Interest Statement

The authors have declared no competing interest.

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 4.0 International license.
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Posted March 02, 2023.
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A conserved pressure-driven mechanism for regulating cytosolic osmolarity
Katrina B. Velle, Rikki M. Garner, Tatihana K. Beckford, Makaela Weeda, Chunzi Liu, Andrew S. Kennard, Marc Edwards, Lillian K. Fritz-Laylin
bioRxiv 2023.03.01.529730; doi: https://doi.org/10.1101/2023.03.01.529730
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A conserved pressure-driven mechanism for regulating cytosolic osmolarity
Katrina B. Velle, Rikki M. Garner, Tatihana K. Beckford, Makaela Weeda, Chunzi Liu, Andrew S. Kennard, Marc Edwards, Lillian K. Fritz-Laylin
bioRxiv 2023.03.01.529730; doi: https://doi.org/10.1101/2023.03.01.529730

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