Cell shape and chromosome partition in prokaryotes or, why <i>E. coli</i> is rod‐shaped and haploid

Donachie, W.; Addinall, Stephen G.; Begg, K J

doi:10.1002/bies.950170616

Cited by 23 publications

(26 citation statements)

References 26 publications

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“…If cell division is resumed, daughter cells are generated that are morphologically indistinguishable from the mother filamentous cell. Similarly, resumption of several rounds of cell division in spherical cells yields spheres of unit size (9).…”

Section: Discussionmentioning

confidence: 99%

Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti

Latch¹,

Margolin²

1997

J Bacteriol

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Inhibition of cell division in rod-shaped bacteria such as Escherichia coli and Bacillus subtilis results in elongation into long filaments many times the length of dividing cells. As a first step in characterizing the Rhizobium meliloti cell division machinery, we tested whether R. meliloti cells could also form long filaments after cell division was blocked. Unexpectedly, DNA-damaging agents, such as mitomycin C and nalidixic acid, caused only limited elongation. Instead, mitomycin C in particular induced a significant proportion of the cells to branch at the poles. Moreover, methods used to inhibit septation, such as FtsZ overproduction and cephalexin treatment, induced growing cells to swell, bud, or branch while increasing in mass, whereas filamentation was not observed. Overproduction of E. coli FtsZ in R. meliloti resulted in the same branched morphology, as did overproduction of R. meliloti FtsZ in Agrobacterium tumefaciens. These results suggest that in these normally rod-shaped species and perhaps others, branching and swelling are default pathways for increasing mass when cell division is blocked.Rod-shaped bacteria such as Escherichia coli grow by elongation and segregate their chromosomes to either side of the future division site (8). When cell division is blocked either directly, as in fts mutants, or indirectly, by treatment with DNA-damaging agents or in strains with mutations affecting DNA synthesis or segregation, cells continue to increase in mass by elongating into filaments many times the length of dividing cells (3). Filamentation in these cases is thought to be due to inhibition of the septation initiator FtsZ or other Fts proteins involved in subsequent steps of cell division (2). A nondividing E. coli cell with intact, segregated chromosomes can be considered a concatemer of unit-length cells which, if division is resumed, can give rise to many cells. Thus, the filamentation process is a way to preserve the architectural and genomic integrity of bipolar unit cells in the predivisional state. Under certain conditions, this maintenance of the bipolar rod shape in bacteria which are normally rod-shaped can be perturbed. Some E. coli cells containing the ftsL mutation form short branches (13). In addition, a small proportion of E. coli cells containing mutations affecting chromosome replication or segregation also can form buds or branches in minimal medium (1). These branches retain the shape characteristics of the mother cell, in particular the diameter. However, it seems clear that at least for E. coli, as well as for many other bacteria, including Bacillus subtilis, the default pathway for growth during cell division inhibition is elongation, not branching.Rhizobium meliloti exists both as a free-living form in the soil and as a nitrogen-fixing bacteroid in leguminous plants (17). Several lines of evidence indicate that its cell division cycle may be different from that of E. coli. First, R. meliloti contains two novel ftsZ genes with divergent C termini; the smaller of the two, ftsZ2, ...

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Section: Discussionmentioning

confidence: 99%

Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti

Latch¹,

Margolin²

1997

J Bacteriol

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“…SHA6 (a rodA (Amber mutant) strain with spherical morphology) carries a duplication of the 0-14 min region of the chromosome which includes the dcw cluster (K. Begg, personal communication; Addinall, 1994;Donachie et al, 1995). In addition, SHA6 carries two functional copies of ftsW (S. G. Addinall, personal communication), therefore, even if ftsW is an essential gene, it should be possible to introduce the ftsW ::cat allele into SHA6 without the need for plasmid-mediated complementation.…”

Section: Identification Of the Promoter Region For Ftswmentioning

confidence: 99%

ftsW is an essential cell‐division gene in Escherichia coli

Boyle

Khattar

Addinall

et al. 1997

Molecular Microbiology

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103

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SummaryIn the absence of exogenous promoters, plasmidmediated complementation of the temperature-sensitive ftsW201 allele requires the presence of the full coding sequence of ftsW plus upstream DNA encompassing the C-terminus of mraY and the full coding sequence of murD. We used molecular and genetic techniques to introduce an insertional inactivation into the chromosomal copy of ftsW, in the presence of the plasmid-borne wild-type ftsW gene under the control of P BAD . In the absence of arabinose, the ftsW-null strain is not viable, and a shift from arabinose-to glucose-containing liquid medium resulted in a block in division, followed by cell lysis. Immunofluorescence microscopy revealed that in ftsW-null filaments, the FtsZ ring is absent in 50-60% of filaments, whilst between one and three Z-rings per filament can be detected in the remainder of the population, with the majority of these containing only one Z-ring per filament. We also demonstrated that the expression of only ftsWS (the smaller of two ftsW open reading frames) from P BAD is sufficient for complementation of the ftsW-null allele. We conclude that FtsW is an essential cell-division protein in Escherichia coli, and that it plays a role in the stabilization of the FtsZ ring during cell division.

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“…The round mutant (rodA) and its parental rod-shaped cell were obtained from K. Begg (9). Any discrepancies between previous work with this mutant and the results reported here are therefore not due to genetic differences.…”

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confidence: 72%

“…This indicates that there is no major reorganization of the division process in the round mutant. Donachie et al (9) had previously concluded that in the round mutant successive planes of division occur at right angles to each other.…”

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Division pattern of a round mutant of Escherichia coli

Cooper

1997

J Bacteriol

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A round mutant of Escherichia coli, when grown in Methocel medium, forms chains of cells and does not form tetrads. This implies that successive division planes of the round mutant are parallel rather than perpendicular. These results differ from a previous proposal that division planes in this round mutant are perpendicular to the prior division plane (W. D. Donachie, S. Addinall, and K. Begg, Bioessays 17:569-576, 1995).When round mutants were originally isolated, they were conditional (temperature-sensitive) cells (10). Recently, Donachie et al. (9) have produced a nonconditional, stable, round mutant of Escherichia coli. They reported that divisions occur with successive planes of division positioned at right angles to each other. This conclusion is derived from the observation that cells growing on agar produced four-cornered tetrads, or square arrangements, at the four-cell stage. Tetrad formation is explained by the alternation of successive division planes, with a division plane occurring perpendicular to the previous division plane. This pattern differs from the parental, rod-shaped cell, where successive division planes are parallel.If the tetrad-forming ability of round cells (due to alternation of planes of division) is real, then there are problems reconciling this growth pattern with the hoop-between-hoop model for normal cell growth. Rod-shaped E. coli cells are believed to grow in the side wall by the insertion of new hoops of peptidoglycan between old hoops (1-4). Hoops run circumferentially around the cell, perpendicular to the long axis. If this peptidoglycan insertion mechanism is retained in the round mutant, then it is difficult to imagine how planes of division can occur perpendicular to the previous division plane. The alternate division plane pattern would entail cutting through, rather than insertion between, preexisting hoops.

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Cell shape and chromosome partition in prokaryotes or, why E. coli is rod‐shaped and haploid

Cited by 23 publications

References 26 publications

Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti

Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti

ftsW is an essential cell‐division gene in Escherichia coli

Division pattern of a round mutant of Escherichia coli

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