Apparent simplicity and emergent robustness in the control of the Escherichia coli cell cycle

IF 9 1区 生物学 Q1 BIOCHEMISTRY & MOLECULAR BIOLOGY Cell Systems Pub Date : 2023-12-28 DOI:10.1016/j.cels.2023.12.001
Sander K. Govers, Manuel Campos, Bhavyaa Tyagi, Géraldine Laloux, Christine Jacobs-Wagner
{"title":"Apparent simplicity and emergent robustness in the control of the Escherichia coli cell cycle","authors":"Sander K. Govers, Manuel Campos, Bhavyaa Tyagi, Géraldine Laloux, Christine Jacobs-Wagner","doi":"10.1016/j.cels.2023.12.001","DOIUrl":null,"url":null,"abstract":"<p>To examine how bacteria achieve robust cell proliferation across diverse conditions, we developed a method that quantifies 77 cell morphological, cell cycle, and growth phenotypes of a fluorescently labeled <em>Escherichia coli</em> strain and &gt;800 gene deletion derivatives under multiple nutrient conditions. This approach revealed extensive phenotypic plasticity and deviating mutant phenotypes were often nutrient dependent. From this broad phenotypic landscape emerged simple and robust unifying rules (laws) that connect DNA replication initiation, nucleoid segregation, FtsZ ring formation, and cell constriction to specific aspects of cell size (volume, length, or added length) at the population level. Furthermore, completion of cell division followed the initiation of cell constriction after a constant time delay across strains and nutrient conditions, identifying cell constriction as a key control point for cell size determination. Our work provides a population-level description of the governing principles by which <em>E. coli</em> integrates cell cycle processes and growth rate with cell size to achieve its robust proliferative capability.</p><p>A record of this paper’s transparent peer review process is included in the <span>supplemental information</span>.</p>","PeriodicalId":54348,"journal":{"name":"Cell Systems","volume":null,"pages":null},"PeriodicalIF":9.0000,"publicationDate":"2023-12-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Cell Systems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1016/j.cels.2023.12.001","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

To examine how bacteria achieve robust cell proliferation across diverse conditions, we developed a method that quantifies 77 cell morphological, cell cycle, and growth phenotypes of a fluorescently labeled Escherichia coli strain and >800 gene deletion derivatives under multiple nutrient conditions. This approach revealed extensive phenotypic plasticity and deviating mutant phenotypes were often nutrient dependent. From this broad phenotypic landscape emerged simple and robust unifying rules (laws) that connect DNA replication initiation, nucleoid segregation, FtsZ ring formation, and cell constriction to specific aspects of cell size (volume, length, or added length) at the population level. Furthermore, completion of cell division followed the initiation of cell constriction after a constant time delay across strains and nutrient conditions, identifying cell constriction as a key control point for cell size determination. Our work provides a population-level description of the governing principles by which E. coli integrates cell cycle processes and growth rate with cell size to achieve its robust proliferative capability.

A record of this paper’s transparent peer review process is included in the supplemental information.

Abstract Image

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
控制大肠杆菌细胞周期的显性简单性和显性稳健性
为了研究细菌如何在不同条件下实现稳健的细胞增殖,我们开发了一种方法,可以量化荧光标记大肠杆菌菌株和 800 基因缺失衍生物在多种营养条件下的 77 种细胞形态、细胞周期和生长表型。这种方法揭示了广泛的表型可塑性,偏离的突变体表型往往依赖于营养物质。从这一广泛的表型景观中,出现了简单而稳健的统一规则(定律),这些规则在群体水平上将 DNA 复制启动、核仁分离、FtsZ 环形成和细胞收缩与细胞大小(体积、长度或附加长度)的特定方面联系起来。此外,在不同菌株和营养条件下,细胞分裂的完成都会在细胞收缩开始后出现恒定的时间延迟,这表明细胞收缩是决定细胞大小的关键控制点。我们的工作在群体水平上描述了大肠杆菌将细胞周期过程和生长速度与细胞大小结合起来以实现其强大增殖能力的管理原理。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Cell Systems
Cell Systems Medicine-Pathology and Forensic Medicine
CiteScore
16.50
自引率
1.10%
发文量
84
审稿时长
42 days
期刊介绍: In 2015, Cell Systems was founded as a platform within Cell Press to showcase innovative research in systems biology. Our primary goal is to investigate complex biological phenomena that cannot be simply explained by basic mathematical principles. While the physical sciences have long successfully tackled such challenges, we have discovered that our most impactful publications often employ quantitative, inference-based methodologies borrowed from the fields of physics, engineering, mathematics, and computer science. We are committed to providing a home for elegant research that addresses fundamental questions in systems biology.
期刊最新文献
pH and buffering capacity: Fundamental yet underappreciated drivers of algal-bacterial interactions What’s driving rhythmic gene expression: Sleep or the clock? Model integration of circadian- and sleep-wake-driven contributions to rhythmic gene expression reveals distinct regulatory principles On knowing a gene: A distributional hypothesis of gene function Acute response to pathogens in the early human placenta at single-cell resolution
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1