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School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia
Correspondence
P. J. Lewis
Peter.Lewis{at}newcastle.edu.au
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Although not all cell-division proteins are conserved, the tubulin homologue FtsZ is present in virtually all bacteria, some chloroplasts and mitochondria from ancient eukaryotes (Gilson & Beech, 2001). FtsZ self-polymerizes to form a ring at mid-cell, driving the invagination of membrane and cell wall throughout cell division (Errington et al., 2003). It is also the first known protein to assemble at new division sites (Errington et al., 2003) and so represents an excellent early marker for the location of cell division. Although it is a cytoplasmic protein, FtsZ assembles as a polymer adjacent to the inside surface of the cytoplasmic membrane in order to lead the coordinated assembly of the division complex comprising a series of cytoplasmic and integral membrane proteins (Errington et al., 2003). FtsZ placement is dependent on the action of the Min and Noc (nucleoid occlusion) systems, which ensure that division occurs at mid-cell and will not bisect a replicating chromosome (Errington et al., 2003; Wu & Errington, 2004; Rothfield et al., 2005).
The mature Bacillus subtilis division complex (the divisome) comprises eight different proteins (Errington et al., 2003; Hamoen et al., 2006; Harry et al., 2006) and many thousands of protein molecules. For example, it is estimated that there are around 50 000 molecules of DivIC per cell during exponential growth (Katis et al., 1997). All of these proteins have been shown to localize to the sites of cell division, and are integral membrane proteins, apart from FtsZ and FtsA (Errington et al., 2003; Hamoen et al., 2006; Harry et al., 2006).
The cytoplasmic membrane is also thought to be important in cell division (see Mileykovskaya & Dowhan, 2005; Matsumoto et al., 2006 for reviews). The major phospholipids found in B. subtilis are phosphatidylglycerol (PG) and phosphatidylethanolamine (PE), although the minor component cardiolipin (CL) is also considered an important membrane lipid due to its packing and non-bilayer formation properties (de Mendoza et al., 2002; Kawai et al., 2004; Matsumoto et al., 2006). Sites of cell division become enriched in CL and PE; this is thought to be related to their ability to form non-bilayer structures that would be important in septation events (Matsumoto et al., 2006). There is now ample evidence that the mid-cell and polar regions have a different lipid profile to the longitudinal regions of the membrane (Binenbaum et al., 1999; Fishov & Woldringh, 1999; Mileykovskaya & Dowhan, 2000; Kawai et al., 2004; Nishibori et al., 2005) and so proteins with specific lipid preferences may show altered localization during cell division. It is also possible that due to the large amount of division-specific protein at mid-cell, other integral membrane proteins could be physically excluded from the mid-cell region during division due to crowding effects.
We have investigated the localization of integral membrane proteins in B. subtilis and found that some, but not all, are transiently diminished/absent from mid-cell around the time of FtsZ-ring assembly. At this stage of the cell cycle, the amount of known division-specific integral membrane protein present at mid-cell would be low. All the proteins investigated were present at mid-cell during the later stages of division when the level of division-specific proteins was at its highest. The specific reduction of proteins from the mid-cell region was also shown to be dependent on division ring formation and not on other processes such as DNA replication, which is also known to occur around mid-cell (Lemon & Grossman, 1998; Migocki et al., 2004). Consistent with studies on the localization of specific lipids, we interpret our data as suggesting that integral membrane proteins migrate into division septa at different rates dependent on their local lipid environment.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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(Gibco-BRL). B. subtilis strains used and constructed in this work are listed in Table 1. Transformation of B. subtilis was carried out by the method of Anagnostopoulous & Spizizen (1961), as modified by Jenkinson (1983). Transformants were selected on nutrient agar containing the appropriate antibiotic (chloramphenicol 5 µg ml–1, spectinomycin 50 µg ml–1). When used to control expression of genes, xylose and IPTG were used at 0.5 % (w/v) and 0.5 mM, respectively, unless otherwise stated. For microscopy and cell measurement experiments, all strains were grown at 37 °C in CH medium as described previously (Davies et al., 2005). FtsZ-depletion experiments were performed by growing cells in CH+0.5 mM IPTG to an OD600 of 0.3, pelleting the cells, then resuspending them in pre-warmed CH medium lacking IPTG. This point was taken as t0 and further samples were taken at the appropriate times as indicated in the text.
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) using the primers Forward 5'-AACAAGCTGGCCTAGGATGGAAGCTATTTTGATG-3' and Reverse 5'-CAACAAGCTTTTTCAATGACCCCCGATATAGT-3'. The resulting product was digested with AvrII and HindIII (sites underlined in primer sequences) and inserted into similarly cut pSG1192 to generate pNG510 (Table 1). secDF was amplified from strain 168 chromosomal DNA using the primers Forward 5'-GAGGATACTCGAGATGAAAAAAGGACG-3' and Reverse 5'-GCCTGATATGAATTCTTGCGCCGA-3'. The resulting product was digested with XhoI and EcoRI and inserted into similarly cut pSG1729 to give pNG534 (Table 1). The integrity of inserts was confirmed by DNA sequencing. These plasmids were used to transform competent B. subtilis strains as listed in Table 1.
Microscopy, image acquisition and analysis.
Microscopy was performed as detailed previously (Davies et al., 2005) by mounting cells on 1.2 % (w/v) agarose pads, followed by imaging with a Zeiss Axioscop 2 fluorescence microscope fitted with a Photometrics Quantix 1401E cooled CCD camera. Cyan fluorescent protein (CFP) fluorescence was visualized with filter set 31044v2, green fluorescent protein (GFP) with set 41018, and yellow fluorescent protein (YFP) with set 41029 (Chroma Technology). Image processing and analysis was performed as described by Johnson et al. (2004) using MetaMorph v6.1.02 software (Molecular Devices). When performing linescans, a line was drawn right around the cell periphery starting at one of the cell poles. In the resulting intensity profile, the mid-cell sites would therefore correspond approximately to the one-quarter and three-quarter points on the x-axes. Final images were prepared for publication using Adobe Photoshop.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). The expression of both fluorescent fusions was driven by the activity of the wild-type promoters, and polar effects of insertion of the fusions into the chromosome were avoided through expression of downstream genes from the xylose-inducible promoter (see Johnson et al., 2004 and Fig. 1A). The pattern of localization for both SdhA and AtpA fusions was heterogeneous, with multiple small regions of fluorescence of varying levels of intensity (see Johnson et al., 2004). Due to this highly varied level of fluorescence around the cytoplasmic membrane, no obvious pattern of low signal at mid-cell was apparent in either of the single-labelled strains. However, we subsequently noticed that a proportion of the cells in the atpA-cfp sdhA-yfp dual-labelled strain BS133 (Table 1) showed much lower levels of signal at the mid-cell site (Fig. 1B). As is clear in the linescan of the cell perimeter shown in Fig. 1(D), the distribution of each fusion was heterogeneous as marked by a series of peaks and troughs, but at the mid-cell region (light and dark grey arrows, Fig. 1C, D) there was a coincident drop in signal intensity for both fusions. These areas, corresponding to simultaneous dips in the signal of dual fluorescent labels at mid-cell, were subsequently termed cleared regions (CRs) and were found to be present in 9.4 % of exponentially growing cells (Table 2). It should be noted that whilst there are many peaks and troughs for the ATP synthase and succinate dehydrogenase signals, the coincident drops in signal representing CRs only occurred at mid-cell (see arrowed cells, Fig. 1B, C).
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; Table 1). p16.7 is an integral membrane protein from the B. subtilis phage 
29 that is involved in phage DNA replication, and has previously been shown to localize around the cell membrane when ectopically expressed (Meijer et al., 2001; Johnson et al., 2004). This protein plays no role in the metabolism of uninfected B. subtilis and so was used to determine if the appearance of CRs was a non-specific effect on integral membrane proteins at the onset of cell division. Strain BS462 containing an N-terminal gfp fusion to secDF along with the atpA-cfp fusion was also constructed (Fig. 2E; Table 1). SecDF, as part of the Sec secretion complex, is involved in protein secretion (Dalbey & Chen, 2004) and so is not directly associated with the same metabolic activities as ATP synthase and succinate dehydrogenase. Therefore, this strain would inform us whether CRs were a phenomenon that occurred with all B. subtilis integral membrane proteins, or just a subset.
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) and shown to be insignificant (not shown). Previous work has also shown that CFP and GFP fusions can be unambiguously localized with little or no signal crossover (Davies & Lewis, 2003) and so strain BS462 was used to colocalize SecDF and ATP synthase.
Fig. 2(B, C, D) shows the results of examination of strain BS441. Surprisingly, there was no evidence that p16.7 formed CRs, and instead a p16.7 signal was seen to concentrate at division sites concomitant with a drop in the SdhA-YFP signal (arrows, Fig. 2B, D). At early stages of cell division around the time that septal invagination was just beginning, p16.7-CFP signals appeared as slight concentrations of signal at mid-cell (red arrows, Fig. 2B, C), that became more intense as the divisome matured (blue arrows, Fig. 2B, D).
Similarly, no evidence for CRs could be found with strain BS462, and as with p16.7, SecDF appeared to localize to septal regions/membrane ingrowths at an earlier stage of cell division than ATP synthase (Fig. 2F, arrows). Thus, the phenomenon of CRs appears to be restricted to a subset of integral membrane proteins currently comprising the ATP synthase and succinate dehydrogenase complexes.
Cleared regions occur early in the division cycle
The occurrence of CRs only at mid-cell sites indicated that they could be connected to the cell division cycle. In order to investigate the role of cell division in the clearing of integral membrane proteins from the mid-cell site, further strains were constructed to contain dual fluorescent protein fusions to either ftsZ and sdhA (BS351; Table 1, Fig. 3A), or ftsZ and atpA (BS352; Table 1). In these strains expression of wild-type FtsZ was dependent on the presence of IPTG, whereas expression of fluorescently tagged FtsZ was dependent on the presence of xylose. Production of wild-type FtsZ was necessary in these strains as the fluorescently tagged protein is not fully functional (Feucht & Lewis, 2001). The strains also contained a fusion to either sdhA or atpA, both of which lie within operons and require the presence of xylose for the expression of genes within the operons downstream of the site of insertion of the fluorescent protein fusion (see Johnson et al., 2004 and Fig. 3A). Titration of strains with IPTG and xylose indicated that an approximately wild-type cell-length distribution, along with acceptable levels of fluorescence, could be obtained with 0.1 mM IPTG and 0.2 % (w/v) xylose. Western blots indicated that the total level of FtsZ (wild-type plus fusion protein) was slightly higher than the wild-type level of FtsZ in the parent strain 168 (Fig. 3F). The mean cell length of BS351 was 4.03±0.96 µm compared to 3.6 µm obtained for the wild-type strain 168 grown in identical conditions by Sharpe et al. (1998). The small difference in mean cell length may be due to the combined levels of FtsZ and FtsZ-YFP being suboptimal in this strain.
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) and BS352 (atpA, ftsZ fusions; Table 1) were grown and examined microscopically. An image of a chain of cells from strain BS351 along with linescans around the perimeter of the marked cells is shown in Fig. 3(B, C, D). For both strains, regions of low membrane signal corresponded with FtsZ division rings (white arrow Fig. 3B, and black arrows Fig. 3C). However, CRs were not present in all cells with visible FtsZ rings (grey arrow Fig. 3B, and black arrows Fig. 3D). In these cells, the SdhA signal can be clearly seen to overlap the FtsZ signal at mid-cell. These results suggested that CRs may occur at a specific stage of the division cycle and so a detailed analysis of CR appearance with FtsZ rings and cell length was conducted (Fig. 3E). Cells were classified as having no detectable FtsZ ring (Fig. 3E) (‘without’, mean cell length 3.12±0.52 µm), an early-stage division ring that appeared as two dots on opposite sides of mid-cell (morphologies first characterized for DivIC by Katis et al. (1997); ‘early’, 3.59±0.49 µm), a mature division ring (‘ring’, 4.70±0.74 µm), or to be in the late stages of cell division (‘dot’, 6.12±0.42 µm). Both the sdhA ftsZ and atpA ftsZ dual-labelled strains had similar proportions of each class, and similar proportions of cells in which CRs were observed and so results are only shown for the sdhA ftsZ strain BS351 in Fig. 3(E). The majority of cells containing CRs were in the early stage of cell division (Fig. 3E, grey columns) indicating that formation of CRs occurred prior to the full assembly of the division complex, which occurs at the ‘ring’ stage of the division cycle. This effect was not observed in all the cells. It may be a specific response to a very short-lived event in the division cycle not fully resolved in our analysis, or the lowering of mid-cell signal may have been much less in some cells than others. Repeated attempts were made to perform time-lapse imaging on strains BS351 and BS352 to definitively establish the timing of CR formation with cell division, but due to the rapid photobleaching of the FtsZ fusion we were unable to obtain usable data. The division complex represents a significant number of protein molecules and it is possible to envisage a situation whereby the assembly of a large number of proteins involved in synthesis of the division septum might exclude other integral membrane proteins, so creating the lowering of signal we observed. However, since CRs occurred at an earlier stage of the division cycle than the full assembly of the division complex, and were not observed for all integral membrane protein fusions, there must be another explanation.
Mid-cell clearing is not due to DNA replication or chromosome segregation cycles
Due to the overlapping nature of the bacterial cell cycle, DNA replication, chromosome segregation and cell division may all be ongoing in the same cell simultaneously. DNA replication occurs in replication factories positioned approximately around the mid-cell point (Lemon & Grossman, 1998; Migocki et al., 2004), and it was possible that CRs coincided with some aspect of the replication or segregation cycles. To investigate this possibility, strain BS426 was constructed (Fig. 4A; Table 1), in which the expression of ftsZ was dependent on induction with IPTG. Thus, by removing IPTG from the medium, FtsZ levels in the cells would drop, resulting in the formation of filaments. In filamentous cells, it is well established that DNA replication and segregation occur normally until the cells grow too large and lyse (e.g. see Fig. 5 in Wu et al., 1995; Lewis et al., 2000). So, if mid-cell clearing was dependent on aspects of the replication and segregation cycles independent of Z-ring formation, CRs should still appear at regular intervals along filaments in this strain.
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). Immediately following resuspension (t0) cells of strain BS426 had a mean cell length of 4.3 µm which is slightly longer than that of the parent strain BS133 (mean 3.3 µm). Titration of FtsZ levels in strain BS426 was attempted to achieve a mean cell length closer to that of BS133, but increasing or decreasing IPTG levels (0.1–1 mM) did not result in improved mean cell lengths, and the most homogeneous cell-length distributions were obtained using 0.5 mM (not shown).
The frequency of CRs was slightly lower in BS426 compared to BS133 (6.3 % and 9.4 %, respectively; Table 2). In addition, the mean cell length for cells containing CRs was determined as well as the relative position of the CR along the long axis of the cell, where a measurement of 0.5 indicates the mid-point. The mean length at which CRs appeared in BS133 was 4.2±0.49 µm with a relative position of 0.52±0.03, and in BS426 was 5.6±0.9 µm with a relative position of 0.51±0.04. Therefore, although cells of strain BS426 were slightly longer than the parent strain, CRs still formed in the same relative position, indicating that the mechanism affecting this phenomenon was operating normally in these cells.
Following resuspension in IPTG-free medium, strain BS426 continued to grow as indicated by the exponential increase in mean cell length over the 180 min time-course when cells increased in mean length from 4.3 to 23.3 µm (Table 2). As the mean cell length increased, the frequency of CRs (classified for these cells as concomitant drops in fluorescent signals at regular intervals along filaments rather than a single region at mid-cell) decreased so that by 90 min (mean cell length 9.1 µm) no more could be detected at mid-cell or any other position along the cell length, indicating the dependence of CR formation on ftsZ expression and that this phenomenon was not dependent on DNA replication or segregation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Thus, it does not appear that size is the criterion for temporary absence of certain proteins at mid-cell during cell division. Nevertheless, it was observed that septa containing GFP-SecDF were visible before the AtpA-CFP fusion (see arrows, Fig. 2F), which may indicate that although both complexes are large, the ATP synthase complex diffuses more slowly than SecYEG/SecDFYajC. We also investigated the possibility that CRs may be due to some aspect of DNA metabolism, as DNA replication has also been shown to occur around the mid-cell region. However, in strains depleted of FtsZ, in which cells became filamentous but underwent normal DNA replication and segregation, CR frequency rapidly dropped to zero, indicating that CRs were dependent in some way on cell division.
Quantitative analysis showed that CRs only occurred at the early stages of the division cycle, corresponding approximately to the time at which FtsZ rings first assemble. It had seemed possible that the physical crowding by division-specific proteins could be responsible for a passive exclusion of other proteins from the mid-cell. Two lines of evidence suggest this is not the case. Firstly, during the later stages of cell division when the level of division proteins is highest at mid-cell, CRs are not observed. They are only seen at the early stages of division when the mature divisome is still being assembled. Secondly, CRs were not observed with all integral membrane proteins suggesting they may represent a specific response by a subset of proteins.
It was also possible that the lipid composition of the membrane plays a role in CR formation, and there does appear to be a connection between local changes in lipid composition and cell division (Mileykovskaya & Dowhan, 2005). A number of studies in both E. coli and B. subtilis using membrane- and CL-specific dyes indicate that mid-cell and polar regions have a different staining profile to cell-cylinder membrane, and are particularly rich in CL and PE (Fishov & Woldringh, 1999; Mileykovskaya & Dowhan, 2000; Kawai et al., 2004; Nishibori et al., 2005). There is some evidence that ATP synthase is associated with PG domains (Ksenzenko & Brusilow, 1993), which are less abundant at sites of cell division. It could be that due to interaction with different subsets of lipids/lipid domains, some proteins/complexes are more mobile than others in the membrane and can diffuse into newly synthesized membranes before others (e.g. p16.7 and SecDF). Also, the enzymes responsible for synthesis of PE and CL localize to the division septum, where lipid synthesis is thought to occur (Nishibori et al., 2005), and this may inhibit the rate of diffusion of proteins embedded within PG-rich domains into the septal regions.
So, are CRs due to active exclusion or passive diffusion? The former is unlikely, as if that was the case, we would have expected to see them clearly in every cell early during the division cycle, whereas they were only seen in about 40 % of cells at the early stages of cell division. It seems more likely that CRs are due to a slower rate of diffusion of certain complexes into newly synthesized membrane at the onset of cell division. The juxtaposition of membrane domains to centre cell at the onset of division could affect how easily detected a CR is, hence they are only seen in about 40 % of cells early in the division cycle. Nevertheless, CRs could be indicative of local changes in the membrane composition at mid-cell, which are important in the formation of an active divisome that may be important in targeting division proteins to that region of the cell.
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ACKNOWLEDGEMENTS |
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Edited by: B. Margolin
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Received 14 September 2007;
revised 14 October 2007;
accepted 18 October 2007.
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