Precise regulation of the relative rates of surface area and volume synthesis in bacterial cells growing in dynamic environments

被引:28
作者
Shi, Handuo [1 ]
Hu, Yan [1 ]
Odermatt, Pascal D. [1 ,2 ]
Gonzalez, Carlos G. [3 ]
Zhang, Lichao [4 ]
Elias, Joshua E. [4 ]
Chang, Fred [2 ]
Huang, Kerwyn Casey [1 ,4 ,5 ]
机构
[1] Stanford Univ, Dept Bioengn, Stanford, CA 94305 USA
[2] Univ Calif San Francisco, Dept Cell & Tissue Biol, San Francisco, CA 94143 USA
[3] Stanford Univ, Sch Med, Dept Chem & Syst Biol, Stanford, CA 94305 USA
[4] Chan Zuckerberg Biohub, Stanford, CA 94305 USA
[5] Stanford Univ, Sch Med, Dept Microbiol & Immunol, Stanford, CA 94305 USA
基金
瑞士国家科学基金会;
关键词
D O I
10.1038/s41467-021-22092-5
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The steady-state size of bacterial cells correlates with nutrient-determined growth rate. Here, we explore how rod-shaped bacterial cells regulate their morphology during rapid environmental changes. We quantify cellular dimensions throughout passage cycles of stationary-phase cells diluted into fresh medium and grown back to saturation. We find that cells exhibit characteristic dynamics in surface area to volume ratio (SA/V), which are conserved across genetic and chemical perturbations as well as across species and growth temperatures. A mathematical model with a single fitting parameter (the time delay between surface and volume synthesis) is quantitatively consistent with our SA/V experimental observations. The model supports that this time delay is due to differential expression of volume and surface-related genes, and that the first division after dilution occurs at a tightly controlled SA/V. Our minimal model thus provides insight into the connections between bacterial growth rate and cell shape in dynamic environments. Bacterial cells actively change their size and shape in response to external environments. Here, Shi et al. explore how cells regulate their morphology during rapid environmental changes, showing that the characteristic dynamics of surface area-to-volume ratio are conserved across genetic and chemical perturbations, as well as across species and growth temperatures.
引用
收藏
页数:13
相关论文
共 52 条
[11]   MreB actin-mediated segregation of a specific region of a bacterial chromosome [J].
Gital, Z ;
Dye, NA ;
Reisenauer, A ;
Wachi, M ;
Shapiro, L .
CELL, 2005, 120 (03) :329-341
[12]   Relative Rates of Surface and Volume Synthesis Set Bacterial Cell Size [J].
Harris, Leigh K. ;
Theriot, Julie A. .
CELL, 2016, 165 (06) :1479-1492
[13]   A Caulobacter MreB mutant with irregular cell shape exhibits compensatory widening to maintain a preferred surface area to volume ratio [J].
Harris, Leigh K. ;
Dye, Natalie A. ;
Theriot, Julie A. .
MOLECULAR MICROBIOLOGY, 2014, 94 (05) :988-1005
[14]   Simultaneous regulation of cell size and chromosome replication in bacteria [J].
Ho, Po-Yi ;
Amir, Ariel .
FRONTIERS IN MICROBIOLOGY, 2015, 6
[15]   Novel S-benzylisothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shape-determining protein(s) other than penicillin-binding protein 2 [J].
Iwai, N ;
Nagai, K ;
Wachi, M .
BIOSCIENCE BIOTECHNOLOGY AND BIOCHEMISTRY, 2002, 66 (12) :2658-2662
[16]   MECHANISM OF ACTION OF FOSFOMYCIN (PHOSPHONOMYCIN) [J].
KAHAN, FM ;
KAHAN, JS ;
CASSIDY, PJ ;
KROPP, H .
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES, 1974, 235 (MAY10) :364-386
[17]   Decoupling of Rates of Protein Synthesis from Cell Expansion Leads to Supergrowth [J].
Knapp, Benjamin D. ;
Odermatt, Pascal ;
Rojas, Enrique R. ;
Cheng, Wenpeng ;
He, Xiangwei ;
Huang, Kerwyn Casey ;
Chang, Fred .
CELL SYSTEMS, 2019, 9 (05) :434-+
[18]   Mechanisms of Intracellular Scaling [J].
Levy, Daniel L. ;
Heald, Rebecca .
ANNUAL REVIEW OF CELL AND DEVELOPMENTAL BIOLOGY, VOL 28, 2012, 28 :113-135
[19]   ELECTRON MICROSCOPY OF FISSION YEAST SCHIZOSACCHAROMYCES POMBE [J].
MACLEAN, N .
JOURNAL OF BACTERIOLOGY, 1964, 88 (05) :1459-&
[20]   ppGpp:: a global regulator in Escherichia coli [J].
Magnusson, LU ;
Farewell, A ;
Nyström, T .
TRENDS IN MICROBIOLOGY, 2005, 13 (05) :236-242