DNA replication initiation, doubling of rate of phospholipid synthesis, and cell division in Escherichia coli

Joseleau‐Petit, Danièle; Képès, François; Peutat, L; D’Ari, Richard; Képès, Adam

doi:10.1128/jb.169.8.3701-3706.1987

Cited by 29 publications

(16 citation statements)

References 22 publications

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“…The initiation of DNA replication took place about 20 min after division, as determined both by [3H]thymidine pulses (Fig. 4) (14). Furthermore, when replication initiation is blocked, ftsZ expression is stimulated (24).…”

Section: Discussionmentioning

confidence: 99%

Transcription of the ftsZ gene and cell division in Escherichia coli

1990

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TheftsZ gene of Escherichia coli, which lies in a cluster of cell division genes at 2 min on the genetic map, codes for a protein which is thought to play a key role in triggering cell division. Using an ftsZ::lacZ operon fusion, we have studied the transcription of the ftsZ gene under conditions in which cell division was either inhibited or synchronized in the bacterial population. InftsZ, ftsA, ftsQ, and ftsl (or pbpB) mutants, there was no change in the differential rate of expression of the ftsZ gene in nonpermissive conditions, when cell division was completely blocked. Although the FtsZ protein is thought to be limiting for cell division, in synchronized cultures theftsZ gene was expressed not only at the moment of septation initiation but throughout the cell cycle. Its expression, however, was not exponential but linear, with a rapid doubling in rate at a specific cell age; this age, about 20 min after division in a 60-min cycle, was different from the age at which the ftsZ::lacZ operon was duplicated. However, it was close to the age at which replication initiated and at which the rate of phospholipid synthesis doubled. During the transient division inhibition after a nutritional shift-up, ftsZ transcription again became linear, with two doublings in rate at intervals equal to the mass doubling time in the rich medium; it adopted the exponential rate typical of rich medium about 60 min after the shift-up, just before the bacterial population resumed cell division. The doubling in the rate of ftsZ transcription once per cycle in synchronized cultures and once per mass doubling time during the transition period after a nutritional shift-up reflects a new cell cycle event.Although a large number of apparent cell division genes have been identified in Escherichia coli and many have been cloned and sequenced, little is known of the precise role of their products (4). The ftsI (or pbpB) gene product, penicillin-binding protein 3, is the only one for which an activity is known (11).Considerable work has been done on one of these division genes, the ftsZ gene, for which a unique temperaturesensitive allele, ftsZ84, provided the demonstration of its role in an early stage of cell division, possibly the initiation of septum formation (22,33). Further evidence for a direct role of the FtsZ protein in septation was provided by the observation (12, 21) that it is the target of the division inhibitor SfiA (or SulA), whose expression is induced by DNA damage as part of the SOS response (9, 10); in this role, FtsZ is a key element of a system coupling cell division to DNA replication.TheftsZ gene lies in a cluster of cell division genes located at 2 min on the E. coli genetic map (22). Its transcriptional organization is complex, with promoters situated in the coding sequences of the adjacentftsA andftsQ genes (29,32,35,36) (see Fig. 1), suggesting possible regulatory interactions among the products of these three genes; certain authors have postulated the existence of a septation complex including all of these protein...

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Section: Discussionmentioning

confidence: 99%

Transcription of the ftsZ gene and cell division in Escherichia coli

1990

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“…A pulse-chase methodology was used in this experiment (23,32,36). Each strain was grown in continuous culture with succinate mineral salts medium prior to the experiment.…”

Section: Methodsmentioning

confidence: 99%

Phospholipid biosynthesis and solvent tolerance in Pseudomonas putida strains

1997

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The role of the cell envelope in the solvent tolerance mechanisms of Pseudomonas putida was investigated. The responses of a solvent-tolerant strain, P. putida Idaho, and a solvent-sensitive strain, P. putida MW1200, were examined in terms of phospholipid content and composition and of phospholipid biosynthetic rate following exposure to a nonmetabolizable solvent, o-xylene. Following o-xylene exposure, P. putida MW1200 exhibited a decrease in total phospholipid content. In contrast, P. putida Idaho demonstrated an increase in phospholipid content 1 to 6 h after exposure. Analysis of phospholipid biosynthesis showed P. putida Idaho to have a higher basal rate of phospholipid synthesis than MW1200. This rate increased significantly following exposure to xylene. Both strains showed little significant turnover of phospholipid in the absence of xylene. In the presence of xylene, both strains showed increased phospholipid turnover. The rate of turnover was significantly greater in P. putida Idaho than in P. putida MW1200. These results suggest that P. putida Idaho has a greater ability than the solvent-sensitive strain MW1200 to repair damaged membranes through efficient turnover and increased phospholipid biosynthesis.

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“…After this loss of labeled pole (i.e., the third generation of elution and beyond), it should be possible to measure the rate of side wall synthesis. To be precise, the side wall synthesis being measured is the wall being synthesized in the culture during the period of labeling and prior to being placed on (9,10). This doubling has been proposed to represent a doubling in membrane synthetic sites, possibly related to the appearance of periseptal annuli, but no temporal connection has been found (11).…”

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“…Turning now to the pattern of membrane synthesis, over the past two decades there have been many proposals regarding the pattern of membrane synthesis during the division cycle (9,10,15,16). The previous proposals have not related membrane synthesis to the pattern of peptidoglycan synthesis during the division cycle.…”

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Synthesis of peptidoglycan and membrane during the division cycle of rod-shaped, gram-negative bacteria

1993

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A modified procedure for determining the pattern of peptidoglycan synthesis during the division cycle has allowed the measurement of the rate of side wall synthesis during the division cycle without the contribution due to pole formation. As predicted by a model proposing that the surface growth of the cell is regulated by mass increase, we find a decrease in side wall synthesis in the latter half of the division cycle. This supports the proposal that, upon invagination, pole growth accommodates a significant proportion of the increasing cell mass and that residual side wall growth occurs in response to the residual mass increase not accommodated by pole volume. The observed side wall synthesis patterns support the proposal that mass increase is a major, and possibly sole, regulator of bacterial surface increase. Membrane synthesis during the division cycle of the gram-negative, rod-shaped bacteria Escherichia coli and Salmonella typhimurium has also been measured with similar methods. The rate of membrane synthesis-measured by incorporation of radioactive glycerol or palmitate relative to simultaneous labeling with radioactive leucine exhibits the same pattern as peptidoglycan synthesis. The results are compatible with a model of cell surface growth containing the following elements. (i) During the period of the division cycle prior to invagination, growth of the cell occurs predominantly in the side wall and the cell grows only in length. (ii) When invagination begins, pole growth accommodates some cytoplasmic increase, leading to a concomitant decrease in side wall synthesis. (iii) Surface synthesis increases relative to mass synthesis during the last part of the division cycle because of pole formation. It is proposed here that membrane synthesis passively follows the pattern of peptidoglycan synthesis during the division cycle.How is the rate of cell surface synthesis regulated in bacteria? One proposal consistent with the available data is that the surface of the gram-negative, rod-shaped cell grows in response to the increase in cell mass. This proposal has been termed the surface stress model (12; see reference 13 for discussion and recent references). The continuous increase in the cytoplasmic constituents of a cell (RNA, protein, water, and ions, etc.) leads to an increase in turgor pressure on the cell surface. This increase in turgor pressure leads to the stressing and bending of peptidoglycan bonds. The cell surface expands when nascent material is incorporated into the stress-bearing plane upon the preferential scission of the stressed peptidoglycan linkages. Thereby, new wall growth responds to and accommodates the increase in mass or volume. The slight reduction in turgor resulting from the incorporation of new material into the stressed layer allows cell mass to again increase prior to further surface growth. The continuous and exponential increase in cell mass or cytoplasm leads to the continuous increase in cell surface.It has been proposed that the murein of gram-negative, rod-shaped bacteria...

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DNA replication initiation, doubling of rate of phospholipid synthesis, and cell division in Escherichia coli

Cited by 29 publications

References 22 publications

Transcription of the ftsZ gene and cell division in Escherichia coli

Transcription of the ftsZ gene and cell division in Escherichia coli

Phospholipid biosynthesis and solvent tolerance in Pseudomonas putida strains

Synthesis of peptidoglycan and membrane during the division cycle of rod-shaped, gram-negative bacteria

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