There are difficulties with all published models that attempt to explain how rod-shaped bacteria locate their midpoint in preparation for the next cell division. Many bacteria find their middle quite accurately. This evenness of partition has been measured cytologically and is implied by the persistence of synchrony under certain circumstances. Previously, a number of models for the control of cell division have been proposed based on aspects of molecular genetics, ultrastructure measurements, or biochemical kinetics. This paper points out that none of the models in spite of their quite different natures can explain the precision of the location of the division site. Here, the ‘Central Stress Model’ is proposed which depends on the partition of wall tension between the cytoplasmic membrane (CM) and the murein layer in such a way that the CM at the centre of the rod experiences a higher stress than near the poles and that this peak stress increases through the cell cycle. The model assumes that: (i) murein is not incorporated at an established pole but is incorporated diffusely over the sidewall and intensely at sites of cell constriction; (ii) CM is synthesized over the entire cell wall; (iii) the murein and CM layers are attached non-covalently to each other, and interact physically with each other; (iv) this differential location of synthesis leads to a ‘tug-of-war’ that creates differential stresses that peak at the cell centre. Because of the fluid nature of the phospholipid bilayer there is a flux of lipid from the established poles towards the cell centre as the murein sidewall elongates. The flux from the pole lowers the tension in the CM at the ends of the sidewalls and creates a peak tension in the centre. Cells also have a discontinuity in the stresses in the murein at the junction of the curved pole with the cylindrical region of the cell wall (a doubling of the hoop stress above the axial stress). Thus in addition to the midpoint of the cell, these junctions between the polar caps and the cylindrical part of the cell wall are characterized by an abrupt change in the surface stress and we suggest that this can trigger cell division at these junctions to form a chromosome-less minicell. Two other assumptions of the model are that the cell has a membrane-associated system to sense the stress, and to trigger cell division locally when a threshold has been reached. It is suggested that there is a special two-component sensory system responding to tension in the CM. As the cell cycle progresses, and the stress in the centre of the cell exceeds some threshold, a system molecule triggers a cell division event at that site. Like other two-component systems, the sensory component of this two-component system is assumed to be distributed all over the CM. It is also assumed that when the sensory component is triggered it also causes local changes that ensure that division occurs at that site. Consequently, this model can explain why sister cells have very nearly the same size (length, volume, or biomass) and why genes that control a mechanism that senses cell size and initiates cell division have never been identified because they may not exist.
BloomM.,
EvansE.,
MouritsenO.G.1991; Physical properties of the fluid lipid-bilayer components of the cell membrane: a perspective.. Q Rev Biophys 24:293–397
de BoerP.,
CrossleyR.E.,
RothfieldL.I.1989; A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli.. Cell 56:641–649
BurdettI.D.J.,
HigginsM.H.1978; Study of pole assembly in Bacillus subtilisby computer reconstruction of septal growth zones seen in central longitudinal thin sections of cell.. J Bacterial 133:959–971
CookW.R.,
MacAlisterT.J.,
RothfieldL.I.1986; Compartmentalization of the periplasmic space at division sites in gram-negative bacteria.. J Bacteriol 168:1430–1438
CookW.R.,
KepesF.,
Joseleau-PetitD.,
MacAlisterT.J.,
RothfieldL.I.1987; Proposed mechanism for the generation and localization of new division sites during the division cycle of Escherichia coli.. Proc Natl Acad Sci USA847144–7148
DonachieW.D.,
BeggK.J.,
SullivanN.F.1984; The morphogenes of Escherichia coli.. In Microbial Development pp. 27–62 Edited by
LosickR.,
ShapiroL.
Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
GailyD.,
BrayK.,
CooperS.1993; Synthesis of peptidoglycan and membrane during the division cycle of rod-shaped, gramnegative bacteria.. J Bacteriol 175:3121–3130
GroverN.B.,
WoldringhC.L.,
KoppesL.J.H.1987; Elongation and surface extension of individual cells of Escherichia coliB/r: comparison of theoretical and experimental size distributions.. J Theor Biol 129:337–348
HöltjeJ.-V.1993; The three-for-one model.. In Bacterial Growth and Lysis: Metabolism and Structure of the Bacterial Sacculus pp. 419–426 Edited by
de PedroM. A.,
HöltjeJ.-V.,
LöffelhardtW.
New York: Plenum Press;
KellA.,
GlaserR.W.1993; On the mechanical and dynamic properties of plant cell membranes: their role in growth, direct gene transfer and protoplast fusion.. J Theor Biol 160:41–62
KochA.L.,
MobleyH.L.T.,
DoyleR.J.,
StreipsU.N.1981; The coupling of wall growth and chromosome replication in Grampositive rods.. FEMS Microbiol Lett 12:201–208
MacAlisterT.J.,
MacDonaldB.,
RothfieldL.I.1983; The periseptal annulus: an organelle associated with cell division in Gram-negative bacteria.. Proc Natl Acad Sci USA801372–1376
von MeyenburgK.,
HansenF.G.1987; Regulation of chromosomal replication.. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 1555–1577 Edited by
NeidhardtF.C.,
IngrahamJ.L.,
Brooks LowK.,
MagasanikB.,
SchaechterM.,
UmbargerH. E.
Washington, DC: American Society for Microbiology;
MulderE.,
WoldringhC.L.1993; Plasmolysis bays in Escherichia coli: are they related to development and positioning of division sites?. J Bacteriol 175:2241–2247
NorrisV.1992; Phospholipid domains determine the spatial organisation of the Escherichia colicell cycle: the membrane tectonics model.. J Theor Biol 154:91–107
OgdenG.B.,
PrattM.J.,
SchaechterM.1988; The replicative origin of the Escherichia colichromosome binds to the membranes only when hemimethylated.. Cell 54:127–135
SanchezM.,
ValenciaA.,
FerrándizM.-H.,
SanderC.,
VicenteM.1994; Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family.. EMBO J 13:4919–4925
SchwarzH.,
KochA.L.1995; Phase and electron microscopic observations of osmotically induced wrinkling and the role of endocytotic vesicles in the plasmolysis of the Gram-negative cell wall.. Microbiology 141:3161–3170
SurretteM.G.,
StockJ.B.1994; Transmembrane signal transducing proteins.. In Bacterial Cell Wall pp. 465–484 Edited by
GhuysenJ.-M.,
HakenbeckR.
Amsterdam: Elsevier;
Van HelvoortL.M.,
JoopM.L.,
WoldringhC.L.1994; Nucleoid partitioning in Escherichia coliduring steady state growth and recovery from chloramphenicol treatment.. Mol Microbiol 13:577–583
WoldringhC.L.,
MulderE.,
HulsP.G.,
VischerN.1991; Toporegulation of bacterial division according the nucleoid occlusion model.. Res Microbiol 142:309–320