Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells
Many organisms, including yeast cells, bacteria, nematodes, and tardigrades, endure harsh environmental conditions, such as nutrient scarcity, or lack of water and energy for a remarkably long time. The rescue programs that these organisms launch upon encountering these adverse conditions include re...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-11-01
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| Series: | Frontiers in Physics |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fphy.2018.00131/full |
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| author | Shada Abuhattum Shada Abuhattum Kyoohyun Kim Titus M. Franzmann Anne Eßlinger Daniel Midtvedt Raimund Schlüßler Stephanie Möllmert Hui-Shun Kuan Hui-Shun Kuan Simon Alberti Vasily Zaburdaev Vasily Zaburdaev Jochen Guck |
| author_facet | Shada Abuhattum Shada Abuhattum Kyoohyun Kim Titus M. Franzmann Anne Eßlinger Daniel Midtvedt Raimund Schlüßler Stephanie Möllmert Hui-Shun Kuan Hui-Shun Kuan Simon Alberti Vasily Zaburdaev Vasily Zaburdaev Jochen Guck |
| author_sort | Shada Abuhattum |
| collection | DOAJ |
| description | Many organisms, including yeast cells, bacteria, nematodes, and tardigrades, endure harsh environmental conditions, such as nutrient scarcity, or lack of water and energy for a remarkably long time. The rescue programs that these organisms launch upon encountering these adverse conditions include reprogramming their metabolism in order to enter a quiescent or dormant state in a controlled fashion. Reprogramming coincides with changes in the macromolecular architecture and changes in the physical and mechanical properties of the cells. However, the cellular mechanisms underlying the physical–mechanical changes remain enigmatic. Here, we induce metabolic arrest of yeast cells by lowering their intracellular pH. We then determine the differences in the intracellular mass density and stiffness of active and metabolically arrested cells using optical diffraction tomography (ODT) and atomic force microscopy (AFM). We show that an increased intracellular mass density is associated with an increase in stiffness when the growth of yeast is arrested. However, increasing the intracellular mass density alone is not sufficient for maintenance of the growth-arrested state in yeast cells. Our data suggest that the cytoplasm of metabolically arrested yeast displays characteristics of a solid. Our findings constitute a bridge between the mechanical behavior of the cytoplasm and the physical and chemical mechanisms of metabolically arrested cells with the ultimate aim of understanding dormant organisms. |
| first_indexed | 2024-12-20T03:49:16Z |
| format | Article |
| id | doaj.art-5b14626c1aba4cfab0151420966c937b |
| institution | Directory Open Access Journal |
| issn | 2296-424X |
| language | English |
| last_indexed | 2024-12-20T03:49:16Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physics |
| spelling | doaj.art-5b14626c1aba4cfab0151420966c937b2022-12-21T19:54:30ZengFrontiers Media S.A.Frontiers in Physics2296-424X2018-11-01610.3389/fphy.2018.00131417458Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast CellsShada Abuhattum0Shada Abuhattum1Kyoohyun Kim2Titus M. Franzmann3Anne Eßlinger4Daniel Midtvedt5Raimund Schlüßler6Stephanie Möllmert7Hui-Shun Kuan8Hui-Shun Kuan9Simon Alberti10Vasily Zaburdaev11Vasily Zaburdaev12Jochen Guck13Biotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, GermanyJPK Instruments AG, Berlin, GermanyBiotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyDepartment of Applied Physics, Chalmers University of Technology, Gothenburg, SwedenBiotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, GermanyBiotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, GermanyDepartment of Biology, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyMax Planck Institute for the Physics of Complex Systems, Dresden, GermanyDepartment of Biology, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, GermanyBiotechnology Center, Center for Molecular and Cellular Bioengineering, Technische Universität Dresden, Dresden, GermanyMany organisms, including yeast cells, bacteria, nematodes, and tardigrades, endure harsh environmental conditions, such as nutrient scarcity, or lack of water and energy for a remarkably long time. The rescue programs that these organisms launch upon encountering these adverse conditions include reprogramming their metabolism in order to enter a quiescent or dormant state in a controlled fashion. Reprogramming coincides with changes in the macromolecular architecture and changes in the physical and mechanical properties of the cells. However, the cellular mechanisms underlying the physical–mechanical changes remain enigmatic. Here, we induce metabolic arrest of yeast cells by lowering their intracellular pH. We then determine the differences in the intracellular mass density and stiffness of active and metabolically arrested cells using optical diffraction tomography (ODT) and atomic force microscopy (AFM). We show that an increased intracellular mass density is associated with an increase in stiffness when the growth of yeast is arrested. However, increasing the intracellular mass density alone is not sufficient for maintenance of the growth-arrested state in yeast cells. Our data suggest that the cytoplasm of metabolically arrested yeast displays characteristics of a solid. Our findings constitute a bridge between the mechanical behavior of the cytoplasm and the physical and chemical mechanisms of metabolically arrested cells with the ultimate aim of understanding dormant organisms.https://www.frontiersin.org/article/10.3389/fphy.2018.00131/fullyeastoptical diffraction tomographyatomic force microscopyrefractive indexstiffnessliquid solid transition |
| spellingShingle | Shada Abuhattum Shada Abuhattum Kyoohyun Kim Titus M. Franzmann Anne Eßlinger Daniel Midtvedt Raimund Schlüßler Stephanie Möllmert Hui-Shun Kuan Hui-Shun Kuan Simon Alberti Vasily Zaburdaev Vasily Zaburdaev Jochen Guck Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells Frontiers in Physics yeast optical diffraction tomography atomic force microscopy refractive index stiffness liquid solid transition |
| title | Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells |
| title_full | Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells |
| title_fullStr | Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells |
| title_full_unstemmed | Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells |
| title_short | Intracellular Mass Density Increase Is Accompanying but Not Sufficient for Stiffening and Growth Arrest of Yeast Cells |
| title_sort | intracellular mass density increase is accompanying but not sufficient for stiffening and growth arrest of yeast cells |
| topic | yeast optical diffraction tomography atomic force microscopy refractive index stiffness liquid solid transition |
| url | https://www.frontiersin.org/article/10.3389/fphy.2018.00131/full |
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