Beyond the average: An updated framework for understanding the relationship between cell growth, DNA replication, and division in a bacterial system
Our understanding of the bacterial cell cycle is framed largely by population-based experiments that focus on the behavior of idealized average cells. Most famously, the contributions of Cooper and Helmstetter help to contextualize the phenomenon of overlapping replication cycles observed in rapidly...
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| Published in | PLoS genetics Vol. 19; no. 1; p. e1010505 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
05.01.2023
Public Library of Science (PLoS) |
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| Abstract | Our understanding of the bacterial cell cycle is framed largely by population-based experiments that focus on the behavior of idealized average cells. Most famously, the contributions of Cooper and Helmstetter help to contextualize the phenomenon of overlapping replication cycles observed in rapidly growing bacteria. Despite the undeniable value of these approaches, their necessary reliance on the behavior of idealized average cells masks the stochasticity inherent in single-cell growth and physiology and limits their mechanistic value. To bridge this gap, we propose an updated and agnostic framework, informed by extant single-cell data, that quantitatively accounts for stochastic variations in single-cell dynamics and the impact of medium composition on cell growth and cell cycle progression. In this framework, stochastic timers sensitive to medium composition impact the relationship between cell cycle events, accounting for observed differences in the relationship between cell cycle events in slow- and fast-growing cells. We conclude with a roadmap for potential application of this framework to longstanding open questions in the bacterial cell cycle field. |
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| AbstractList | Our understanding of the bacterial cell cycle is framed largely by population-based experiments that focus on the behavior of idealized average cells. Most famously, the contributions of Cooper and Helmstetter help to contextualize the phenomenon of overlapping replication cycles observed in rapidly growing bacteria. Despite the undeniable value of these approaches, their necessary reliance on the behavior of idealized average cells masks the stochasticity inherent in single-cell growth and physiology and limits their mechanistic value. To bridge this gap, we propose an updated and agnostic framework, informed by extant single-cell data, that quantitatively accounts for stochastic variations in single-cell dynamics and the impact of medium composition on cell growth and cell cycle progression. In this framework, stochastic timers sensitive to medium composition impact the relationship between cell cycle events, accounting for observed differences in the relationship between cell cycle events in slow- and fast-growing cells. We conclude with a roadmap for potential application of this framework to longstanding open questions in the bacterial cell cycle field. |
| Audience | Academic |
| Author | Iyer-Biswas, Srividya Sanders, Sara Levin, Petra Anne Joshi, Kunaal |
| AuthorAffiliation | 3 Santa Fe Institute, Santa Fe, New Mexico, United States of America 1 Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America The University of North Carolina at Chapel Hill, UNITED STATES 2 Department of Physics and Astronomy, Purdue University, West Lafayette, Indiana, United States of America |
| AuthorAffiliation_xml | – name: 2 Department of Physics and Astronomy, Purdue University, West Lafayette, Indiana, United States of America – name: The University of North Carolina at Chapel Hill, UNITED STATES – name: 3 Santa Fe Institute, Santa Fe, New Mexico, United States of America – name: 1 Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America |
| Author_xml | – sequence: 1 givenname: Sara surname: Sanders fullname: Sanders, Sara organization: Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America – sequence: 2 givenname: Kunaal orcidid: 0000-0002-8001-1230 surname: Joshi fullname: Joshi, Kunaal organization: Department of Physics and Astronomy, Purdue University, West Lafayette, Indiana, United States of America – sequence: 3 givenname: Petra Anne surname: Levin fullname: Levin, Petra Anne organization: Department of Biology, Washington University in St. Louis, St. Louis, Missouri, United States of America – sequence: 4 givenname: Srividya orcidid: 0000-0002-1587-6780 surname: Iyer-Biswas fullname: Iyer-Biswas, Srividya organization: Santa Fe Institute, Santa Fe, New Mexico, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36602967$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright: © 2023 Sanders et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2023 Public Library of Science 2023 Sanders et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2023 Sanders et al 2023 Sanders et al |
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| Title | Beyond the average: An updated framework for understanding the relationship between cell growth, DNA replication, and division in a bacterial system |
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