J. theor. Biol. (1992) 154, 91-107
Phospholipid Domains Determine the Spatial Organization of
the Escherichia coil Cell Cycle: the Membrane Tectonics Model
VIC NORRIS
Department of Genetics, University of Leicester, Leicester LE1 7RH, U.K.
(Received on 16 January 1991, Accepted in revised form
on 12 September 1991)
Escherichia coli normally divides at its equator between segregated nucleoids. Such
division is inhibited during perturbations of chromosome replication (even in the
absence of inducible division inhibitors); eventually, division resumes at sites which
are not at this equator. Escherichia coli will also divide at its poles to generate
minicells following overproduction of the FtsZ or MinE proteins. The mechanisms
underlying the division inhibition and the positioning of the division sites are
unknown. In the membrane tectonics model, I propose that the formation of phos-
pholipid domains within the cytoplasmic membrane positions division sites. The
particular phospholipid composition of a domain attracts particular proteins and
determines their activity; conversely, particular proteins change the composition of
domains. Principally via such proteins, the interaction of the chromosome with the
membrane creates a chromosomal domain. The development of chromosomal
domains during replication and nucleoid formation contributes to the formation and
positioning of a septal domain between them. During septation (cell division), this
septal domain matures into a polar domain. Each domain attracts and activates
different enzymes. The septal domain attracts and activates enzymes necessary for
septation. Preventing the formation of the septal domain by preventing chromosome
replication prevents normal division. Altering the composition of the polar domain
may allow septation enzymes to function there and generate minicells. A corollary
of the model explains how the formation of an origin domain by the attachment of
hemi-methylated origin DNA to the membrane may underlie the creation and migra-
tion of structures within the envelope, the periseptal annuli.
Introduction
During the cell cycle of Escherichia coli cells normally divide at the equator between
the segregated nucleoids. This process is tightly controlled and septum formation is
timed and positioned such that daughter cells are of similar sizes and few DNA-less
cells are formed (Jaff6 et al., 1986). Although some components of the mechanism
responsible for this control have been elucidated, the mechanism itself remains
obscure.
In E. coli, the position and development of the constriction site is related to the
position and activity of the chromosomes. Perturbations of chromosome replication
result in an inhibition of cell division due to the synthesis of a division inhibitor,
SfiA (Huisman & D'Ari, 1981 ; Little & Mount, 1982). In the absence of SfiA, cell
division is still inhibited by a "second mechanism" (Huisman et al., 1980; Burton &
Holland, 1983). The nature of this second inhibitory mechanism is unknown. In
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