TY - JOUR
T1 - Size Laws and Division Ring Dynamics in Filamentous Escherichia coli cells
AU - Wehrens, Martijn
AU - Ershov, Dmitry
AU - Rozendaal, Rutger
AU - Walker, Noreen
AU - Schultz, Daniel
AU - Kishony, Roy
AU - Levin, Petra Anne
AU - Tans, Sander J.
N1 - Funding Information:
Work in the group of S.J.T. is supported by the Netherlands Organization for Scientific Research (NWO) . P.A.L. is funded in part by NIH grant GM64671 and a grant from the Fulbright US Scholar Program . R.K is funded by the European Research Council (ERC) FP7 grant 281891 and the NIH grant GM081617 . We thank Svetlana Alexeeva and Tanneke den Blaauwen, Alexander Dajkovic, Cees Dekker, and Suckjoon Jun for kindly sharing their plasmid constructs, Daan J. Kiviet for kindly providing a microfluidic device mold, and Nick de Lange for performing the sulA recovery experiment.
Publisher Copyright:
© 2018 Elsevier Ltd
PY - 2018/3/19
Y1 - 2018/3/19
N2 - Our understanding of bacterial cell size control is based mainly on stress-free growth conditions in the laboratory [1–10]. In the real world, however, bacteria are routinely faced with stresses that produce long filamentous cell morphologies [11–28]. Escherichia coli is observed to filament in response to DNA damage [22–25], antibiotic treatment [11–14, 28], host immune systems [15, 16], temperature [17], starvation [20], and more [18, 19, 21], conditions which are relevant to clinical settings and food preservation [26]. This shape plasticity is considered a survival strategy [27]. Size control in this regime remains largely unexplored. Here we report that E. coli cells use a dynamic size ruler to determine division locations combined with an adder-like mechanism to trigger divisions. As filamentous cells increase in size due to growth, or decrease in size due to divisions, its multiple Fts division rings abruptly reorganize to remain one characteristic cell length away from the cell pole and two such length units away from each other. These rules can be explained by spatiotemporal oscillations of Min proteins. Upon removal of filamentation stress, the cells undergo a sequence of division events, randomly at one of the possible division sites, on average after the time required to grow one characteristic cell size. These results indicate that E. coli cells continuously keep track of absolute length to control size, suggest a wider relevance for the adder principle beyond the control of normally sized cells, and provide a new perspective on the function of the Fts and Min systems. Wehrens, Ershov, et al. report a new size-control mechanism in E. coli cells that have elongated due to stress. Multiple division rings are continuously rearranged in response to growth and division to control daughter cell size when divisions resume. Divisions are spatially controlled by the Min system and temporally by the adder principle.
AB - Our understanding of bacterial cell size control is based mainly on stress-free growth conditions in the laboratory [1–10]. In the real world, however, bacteria are routinely faced with stresses that produce long filamentous cell morphologies [11–28]. Escherichia coli is observed to filament in response to DNA damage [22–25], antibiotic treatment [11–14, 28], host immune systems [15, 16], temperature [17], starvation [20], and more [18, 19, 21], conditions which are relevant to clinical settings and food preservation [26]. This shape plasticity is considered a survival strategy [27]. Size control in this regime remains largely unexplored. Here we report that E. coli cells use a dynamic size ruler to determine division locations combined with an adder-like mechanism to trigger divisions. As filamentous cells increase in size due to growth, or decrease in size due to divisions, its multiple Fts division rings abruptly reorganize to remain one characteristic cell length away from the cell pole and two such length units away from each other. These rules can be explained by spatiotemporal oscillations of Min proteins. Upon removal of filamentation stress, the cells undergo a sequence of division events, randomly at one of the possible division sites, on average after the time required to grow one characteristic cell size. These results indicate that E. coli cells continuously keep track of absolute length to control size, suggest a wider relevance for the adder principle beyond the control of normally sized cells, and provide a new perspective on the function of the Fts and Min systems. Wehrens, Ershov, et al. report a new size-control mechanism in E. coli cells that have elongated due to stress. Multiple division rings are continuously rearranged in response to growth and division to control daughter cell size when divisions resume. Divisions are spatially controlled by the Min system and temporally by the adder principle.
KW - cell size control
KW - division
KW - divisome
KW - Escherichia coli
KW - filamentation
KW - mathematical modeling
KW - microfluidics
KW - Min oscillations
KW - time-lapse microcopy
UR - http://www.scopus.com/inward/record.url?scp=85042592513&partnerID=8YFLogxK
U2 - 10.1016/j.cub.2018.02.006
DO - 10.1016/j.cub.2018.02.006
M3 - Article
C2 - 29502951
AN - SCOPUS:85042592513
SN - 0960-9822
VL - 28
SP - 972-979.e5
JO - Current Biology
JF - Current Biology
IS - 6
ER -