Developmental Control of a<i>parAB</i>Promoter Leads to Formation of Sporulation-Associated ParB Complexes in<i>Streptomyces coelicolor</i>

Jakimowicz, Dagmara; Mouz, Sébastien; Zakrzewska‐Czerwińska, Jolanta; Chater, Keith F.

doi:10.1128/jb.188.5.1710-1720.2006

Cited by 51 publications

(59 citation statements)

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“…The formation of ParB complexes in the aerial hyphae of S. coelicolor is dependent on the developmental induction of the parAB promoter. Thus, ParB complexes were not observed in the nonsporulating (white) Streptomyces mutants (70). Earlier studies showed that in S. coelicolor, as in other bacteria, the ParA protein is required for efficient formation and regularly spaced placement of ParB complexes (42).…”

Section: Discussionmentioning

confidence: 99%

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

et al. 2013

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c Streptomyces species are bacteria that resemble filamentous fungi in their hyphal mode of growth and sporulation. In Streptomyces coelicolor, the conversion of multigenomic aerial hyphae into chains of unigenomic spores requires synchronized septation accompanied by segregation of tens of chromosomes into prespore compartments. The chromosome segregation is dependent on ParB protein, which assembles into an array of nucleoprotein complexes in the aerial hyphae. Here, we report that nucleoprotein ParB complexes are bound in vitro and in vivo by topoisomerase I, TopA, which is the only topoisomerase I homolog found in S. coelicolor. TopA cannot be eliminated, and its depletion inhibits growth and blocks sporulation. Surprisingly, sporulation in the TopA-depleted strain could be partially restored by deletion of parB. Furthermore, the formation of regularly spaced ParB complexes, which is a prerequisite for proper chromosome segregation and septation during the development of aerial hyphae, has been found to depend on TopA. We hypothesize that TopA is recruited to ParB complexes during sporulation, and its activity is required to resolve segregating chromosomes.

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Section: Discussionmentioning

confidence: 99%

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

et al. 2013

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“…SMC complexes are transiently localized at the time of sporulation, when DNA has to be compacted and segregated. Thus, SMC, like FtsZ (8) and ParAB (19,20), seems to belong to the larger group of proteins whose expression is highly induced in response to the requirement of aerial hyphal maturation. The SMC foci, like FtsZ and ParAB, disappear after septation.…”

Section: Discussionmentioning

confidence: 99%

SMC Protein-Dependent Chromosome Condensation during Aerial Hyphal Development in Streptomyces

et al. 2009

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Members of the SMC (structural maintenance of chromosomes) protein family play a central role in higher-order chromosome dynamics from bacteria to humans. So far, studies of bacterial SMC proteins have focused only on unicellular rod-shaped organisms that divide by binary fission. The conversion of multigenomic aerial hyphae of the mycelial organism Streptomyces coelicolor into chains of unigenomic spores requires the synchronous segregation of multiple chromosomes. Here we focus on the contribution of SMC proteins to sporulation-associated chromosome segregation in S. coelicolor. Deletion of the smc gene causes aberrant DNA condensation and missegregation of chromosomes (7.5% anucleate spores). In vegetative mycelium, immunostained SMC proteins were observed sporadically, while in aerial hyphae about to undergo sporulation they appeared as irregularly spaced foci which accompanied but did not colocalize with ParB complexes. Our data demonstrate that efficient chromosome segregation requires the joint action of SMC and ParB proteins. SMC proteins, similarly to ParAB and FtsZ, presumably belong to a larger group of proteins whose expression is highly induced in response to the requirement of aerial hyphal maturation.Higher-order chromosome structure is particularly critical in the segregation of replicated chromosomes during cell division in eubacteria, eukaryotes, and archaea. Recent studies have shown that members of the SMC (structural maintenance of chromosomes) protein family play a central role in higher-order chromosome dynamics, acting either as condensins or cohesins (15-17, 30, 32, 36, 40). SMC are large proteins (110 to 170 kDa) that form dimers. Their N-and C-terminal parts form a single head domain (see references 13, 15-17, and 38 for reviews). SMC proteins exhibit ATPase activity that is required for their dynamic interaction with DNA (17). The results of recent studies demonstrated that bacterial SMC protein functions in complexes with other proteins, i.e., ScpA and ScpB (Scp's are segregation and condensation proteins) (6,29,37).In contrast to eukaryotes, in eubacteria the cell-cycle events, including replication, condensation, and segregation, take place simultaneously (16,26). Thus, during the bacterial cell cycle, chromosomes must undergo dynamic changes. So far, studies regarding chromosome dynamics have focused on Bacillus subtilis, Caulobacter crescentus, and Escherichia coli. In these organisms, SMC proteins (or MukB, a functional homologue in E. coli) appear to play similar roles; they are involved in chromosome organization and segregation. The genes encoding these proteins are not essential, although their deletion results in temperature-sensitive growth (2,9,22,31,32,38). In B. subtilis, smc deletion mutants exhibit complex phenotypes under permissive conditions, including poorly compacted nucleoids and a relatively large amount of anucleate cells (up to 15% of the cells were anucleate) (10). Interestingly, the inactivation of smc enhances the chromosome segregation defect of spo0J-or...

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“…S. coelicolor WhiA binds to its own promoter and is required for its own expression (26,50), the sporulation-dependent expression of ftsZ, and the expression of other sporulation genes (27,51,52). The nucleoidbinding activity of YvcL and its homology to WhiA suggest that YvcL functions as a transcription factor, possibly regulating ftsZ expression.…”

Section: Synthetic Lethal Screenmentioning

confidence: 99%

The Conserved DNA-Binding Protein WhiA Is Involved in Cell Division in Bacillus subtilis

et al. 2013

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e Bacterial cell division is a highly coordinated process that begins with the polymerization of the tubulin-like protein FtsZ at midcell. FtsZ polymerization is regulated by a set of conserved cell division proteins, including ZapA. However, a zapA mutation does not result in a clear phenotype in Bacillus subtilis. In this study, we used a synthetic-lethal screen to find genes that become essential when ZapA is mutated. Three transposon insertions were found in yvcL. The deletion of yvcL in a wild-type background had only a mild effect on growth, but a yvcL zapA double mutant is very filamentous and sick. This filamentation is caused by a strong reduction in FtsZ-ring assembly, suggesting that YvcL is involved in an early stage of cell division. YvcL is 25% identical and 50% similar to the Streptomyces coelicolor transcription factor WhiA, which induces ftsZ and is required for septation of aerial hyphae during sporulation. Using green fluorescent protein fusions, we show that YvcL localizes at the nucleoid. Surprisingly, transcriptome analyses in combination with a ChIP-on-chip assay gave no indication that YvcL functions as a transcription factor. To gain more insight into the function of YvcL, we searched for suppressors of the filamentous phenotype of a yvcL zapA double mutant. Transposon insertions in gtaB and pgcA restored normal cell division of the double mutant. The corresponding proteins have been implicated in the metabolic sensing of cell division. We conclude that YvcL (WhiA) is involved in cell division in B. subtilis through an as-yet-unknown mechanism.

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Developmental Control of aparABPromoter Leads to Formation of Sporulation-Associated ParB Complexes inStreptomyces coelicolor

Cited by 51 publications

References 50 publications

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

SMC Protein-Dependent Chromosome Condensation during Aerial Hyphal Development in Streptomyces

The Conserved DNA-Binding Protein WhiA Is Involved in Cell Division in Bacillus subtilis

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