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Size Laws and Division Ring Dynamics in Filamentous Escherichia coli cells

2018; Elsevier BV; Volume: 28; Issue: 6 Linguagem: Inglês

10.1016/j.cub.2018.02.006

1879-0445

Martijn Wehrens, Dmitry Ershov, Rutger Rozendaal, Noreen Walker, Daniel Schultz, Roy Kishony, Petra Anne Levin, Sander J. Tans,

thermodynamics and calorimetric analyses

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SulA-independent filamentation of Escherichia coli during growth after release from high hydrostatic pressure treatment.Appl. Microbiol. Biotechnol. 2004; 64: 255-262Crossref PubMed Scopus (47) Google Scholar, 20Wainwright M. Canham L.T. al-Wajeeh K. Reeves C.L. Morphological changes (including filamentation) in Escherichia coli grown under starvation conditions on silicon wafers and other surfaces.Lett. Appl. Microbiol. 1999; 29: 224-227Crossref PubMed Scopus (35) Google Scholar, 21Rosenberg B. Renshaw E. Vancamp L. Hartwick J. Drobnik J. Platinum-induced filamentous growth in Escherichia coli.J. Bacteriol. 1967; 93: 716-721PubMed Google Scholar, 22Adler H.I. Hardigree A.A. Growth and division of filamentous forms of Escherichia coli.J. Bacteriol. 1965; 90: 223-226PubMed Google Scholar, 23Kantor G.J. Deering R.A. Ultraviolet radiation studies of filamentous Escherichia coli B.J. Bacteriol. 1966; 92: 1062-1069PubMed Google Scholar, 24Radman M. 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Escherichia coli is observed to filament in response to DNA damage [22Adler H.I. Hardigree A.A. Growth and division of filamentous forms of Escherichia coli.J. Bacteriol. 1965; 90: 223-226PubMed Google Scholar, 23Kantor G.J. Deering R.A. Ultraviolet radiation studies of filamentous Escherichia coli B.J. Bacteriol. 1966; 92: 1062-1069PubMed Google Scholar, 24Radman M. SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis.in: Part A. Hanawalt P. Molecular Mechanisms for Repair of DNA. Springer, 1975: 355-367Crossref Scopus (418) Google Scholar, 25Michel B. After 30 years of study, the bacterial SOS response still surprises us.PLoS Biol. 2005; 3: e255Crossref PubMed Scopus (224) Google Scholar], antibiotic treatment [11Suzuki H. Pangborn J. Kilgore W.W. Filamentous cells of Escherichia coli formed in the presence of mitomycin.J. Bacteriol. 1967; 93: 683-688PubMed Google Scholar, 12Rolinson G.N. Effect of beta-lactam antibiotics on bacterial cell growth rate.J. Gen. Microbiol. 1980; 120: 317-323PubMed Google Scholar, 13Miller C. Thomsen L.E. Gaggero C. Mosseri R. Ingmer H. Cohen S.N. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality.Science. 2004; 305: 1629-1631Crossref PubMed Scopus (425) Google Scholar, 14Domadia P. Swarup S. Bhunia A. Sivaraman J. Dasgupta D. Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde.Biochem. Pharmacol. 2007; 74: 831-840Crossref PubMed Scopus (199) Google Scholar, 28Pulvertaft R.J. The effect of antibiotics on growing cultures of Bacterium coli.J. Pathol. Bacteriol. 1952; 64: 75-89Crossref PubMed Scopus (17) Google Scholar], host immune systems [15Justice S.S. Hunstad D.A. Seed P.C. Hultgren S.J. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection.Proc. Natl. Acad. Sci. USA. 2006; 103: 19884-19889Crossref PubMed Scopus (236) Google Scholar, 16Möller J. Luehmann T. Hall H. Vogel V. The race to the pole: how high-aspect ratio shape and heterogeneous environments limit phagocytosis of filamentous Escherichia coli bacteria by macrophages.Nano Lett. 2012; 12: 2901-2905Crossref PubMed Scopus (78) Google Scholar], temperature [17Jones T. Gill C.O. McMullen L.M. The behaviour of log phase Escherichia coli at temperatures that fluctuate about the minimum for growth.Lett. Appl. Microbiol. 2004; 39: 296-300Crossref PubMed Scopus (39) Google Scholar], starvation [20Wainwright M. Canham L.T. al-Wajeeh K. Reeves C.L. Morphological changes (including filamentation) in Escherichia coli grown under starvation conditions on silicon wafers and other surfaces.Lett. Appl. Microbiol. 1999; 29: 224-227Crossref PubMed Scopus (35) Google Scholar], and more [18Linn S. Imlay J.A. Toxicity, mutagenesis and stress responses induced in Escherichia coli by hydrogen peroxide.J. Cell Sci. Suppl. 1987; 6: 289-301Crossref PubMed Google Scholar, 19Kawarai T. Wachi M. Ogino H. Furukawa S. Suzuki K. Ogihara H. Yamasaki M. SulA-independent filamentation of Escherichia coli during growth after release from high hydrostatic pressure treatment.Appl. Microbiol. Biotechnol. 2004; 64: 255-262Crossref PubMed Scopus (47) Google Scholar, 21Rosenberg B. Renshaw E. Vancamp L. Hartwick J. Drobnik J. Platinum-induced filamentous growth in Escherichia coli.J. Bacteriol. 1967; 93: 716-721PubMed Google Scholar], conditions which are relevant to clinical settings and food preservation [26Jones T.H. Vail K.M. McMullen L.M. Filament formation by foodborne bacteria under sublethal stress.Int. J. Food Microbiol. 2013; 165: 97-110Crossref PubMed Scopus (39) Google Scholar]. This shape plasticity is considered a survival strategy [27Justice S.S. Hunstad D.A. Cegelski L. Hultgren S.J. Morphological plasticity as a bacterial survival strategy.Nat. Rev. Microbiol. 2008; 6: 162-168Crossref PubMed Scopus (404) Google Scholar]. 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.