A <i>Bacillus subtilis</i> gene‐encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition

Moriya, Shigeki; Tsujikawa, Eitoku; Hassan, Anwarul K. M.; Asai, Kei; Kodama, Takeko; Ogasawara, Nagahisa

doi:10.1046/j.1365-2958.1998.00919.x

Cited by 178 publications

(194 citation statements)

References 44 publications

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“…However, LP101 cultures grown without xylose contained significantly more anucleate cells (ϳ24%) than did cultures grown in the presence of xylose (ϳ15% [Table 3]), suggesting that the lack of PrfA exacerbates the smc phenotype. Cultures of smc (LP99) cells grown under similar conditions contained ϳ13% anucleate cells (Table 3), which is consistent with previous reports (ϳ10 to 15% anucleate cells [6,26]). We also examined the LP101 cells grown to stationary phase in PAB medium with or without xylose.…”

Section: Vol 182 2000supporting

confidence: 91%

“…In addition, six so-called par genes involved in decatenation of interlinked daughter chromosomes have been characterized, as well as a number of genes thought to be involved in chromosome movement and partitioning (reviewed in reference 43). Among the latter group are the muk, minD, and ftsK genes of E. coli (12,23,49) and the smc, spoOJ, and spoIIIE genes of B. subtilis (6,13,26,45). Finally, recent work by Lemon and Grossman (19) indicates that the process of DNA replication itself may contribute to the movement and separation of daughter chromosomes.…”

Section: Discussionmentioning

confidence: 99%

“…The smc gene (for "structural maintenance of chromosomes") is required for chromosome structure and partitioning in B. subtilis and inactivation of smc produces cells with chromosome segregation defects similar to but more severe than those observed for prfA cells. For example, smc null mutant cells grown at 23 or 30°C contain about 10 to 15% anucleate cells compared to ϳ0.9 to 3% for prfA cells (Table 3) (6,26). We attempted to generate a prfA smc double mutant by transforming PS2061 (⌬prfA::spc) cells with chromosomal DNA from strain RB35 (⌬smc::kan) and selecting transformants on LB plates supplemented with kanamycin at 30°C (strain RB35 is temperature sensitive for growth in rich medium [6]).…”

Section: Vol 182 2000mentioning

confidence: 99%

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Penicillin-Binding Protein-Related Factor A Is Required for Proper Chromosome Segregation in Bacillus subtilis

Pedersen

Setlow

2000

J Bacteriol

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Previous work has shown that the ponA gene, encoding penicillin-binding protein 1 (PBP1), is in a two-gene operon with prfA (PBP-related factor A) (also called recU), which encodes a putative 206-residue basic protein (pI ‫؍‬ 10.1) with no significant sequence homology to proteins with known functions. Inactivation of prfA results in cells that grow slower and vary significantly in length relative to wild-type cells. We now show that prfA mutant cells have a defect in chromosome segregation resulting in the production of ϳ0.9 to 3% anucleate cells in prfA cultures grown at 30 or 37°C in rich medium and that the lack of PrfA exacerbates the chromosome segregation defect in smc and spoOJ mutant cells. In addition, overexpression of prfA was found to be toxic for and cause nucleoid condensation in Escherichia coli.Penicillin-binding proteins (PBPs), which catalyze the polymerization and cross-linking of bacterial peptidoglycan, can be divided into three classes based on their amino acid sequence: the low-molecular-weight PBPs and the high-molecular-weight (HMW) class A and class B PBPs (8). The HMW class B PBPs are monofunctional transpeptidases, some of which have essential functions in septation and maintenance of cell shape (8), while the HMW class A PBPs have both transglycosylase and transpeptidase activities (14, 42) and appear to be somewhat functionally redundant (17, 34). The Bacillus subtilis ponA gene, coding for the HMW class A PBP1, is transcribed predominantly during log-phase growth (34). Previous work with B. subtilis mutants lacking one or several of the three known HMW class A PBPs (PBP1, PBP2c, and PBP4) showed that (i) lack of PBP1 results in slower growth, increased cell length, and decreased cell diameter and (ii) PBP1 is functionally more important than PBP2c and PBP4 (34). It was also recently demonstrated that PBP1 localizes to cell division sites and plays an important role in the formation of the peptidoglycan division septum in vegetative cells of B. subtilis (30).The ponA gene is part of a two-gene operon that also includes prfA (PBP-related factor A [note that in the B. subtilis genome database, prfA is called recU]), which is located immediately upstream of and cotranscribed with ponA (33). prfA codes for a putative 206 residue, basic protein (pI of 10.1), which has no significant sequence homology to proteins with known functions. However, DNA sequencing has indicated that genes encoding similar proteins are present in a large number of gram-positive bacteria: a BLAST search (2) of prfA against completed and unfinished microbial genomes (preliminary sequence data were obtained from The Institute of Genomic Research Website at http://www.tigr.org) produced sequences with significant homology from 10 different grampositive organisms, while no prfA homologs were detected in gram-negative bacteria by this analysis. The former organisms include Enterococcus faecalis (54% identity in a 192-aminoacid overlap), Staphylococcus aureus (58% identity in a 167-amino-acid overlap), Streptococcus p...

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Section: Vol 182 2000supporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Section: Vol 182 2000mentioning

confidence: 99%

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Penicillin-Binding Protein-Related Factor A Is Required for Proper Chromosome Segregation in Bacillus subtilis

Pedersen

Setlow

2000

J Bacteriol

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“…To generate pMutinT3-ntdR, the DNA fragment containing a ShineDalgarno sequence, and the N-terminal coding region was amplified by PCR with the primers ntdR-F and ntdR-R. A HindIII-BamHI fragment was cloned into pMutinT3 (18), resulting in a plasmid pMutinT3-ntdR.…”

Section: Methodsmentioning

confidence: 99%

RNA Polymerase Mutation Activates the Production of a Dormant Antibiotic 3,3′-Neotrehalosadiamine via an Autoinduction Mechanism in Bacillus subtilis

Inaoka

Takahashi

Yada

et al. 2004

Journal of Biological Chemistry

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Bacillus and Streptomyces species possess the ability to produce a variety of commercially important metabolites and extracellular enzymes. We previously demonstrated that antibiotic production in Streptomyces coelicolor A3(2) and Streptomyces lividans can be enhanced by RNA polymerase (RNAP) mutations selected for the rifampicin-resistant (Rif r ) phenotype. Here, we have shown that the introduction of a certain Rif r rpoB mutation into a B. subtilis strain resulted in cells that overproduce an aminosugar antibiotic 3,3 -neotrehalosadiamine (NTD), the production of which is dormant in the wild-type strain. Mutational and recombinant gene expression analyses have revealed a polycistronic gene ntdABC (formally yhjLKJ) and a monocistronic gene ntdR (formally yhjM) as the NTD biosynthesis operon and a positive regulator for ntdABC, respectively. Analysis of transcriptional fusions to a lacZ reporter revealed that NTD acts as an autoinducer for its own biosynthesis genes via NtdR protein. Our results also showed that the Rif r rpoB mutation causes an increase in the activity of A -dependent promoters including ntdABC promoter. Therefore, we propose that unlike the wild-type RNAP, the mutant RNAP efficiently recognized the A -dependent promoters, resulting in the dramatic activation of the NTD biosynthesis pathway by an autoinduction mechanism.The ability of bacteria to survive in a wide range of adverse environmental conditions depends on diverse molecular mechanisms that adjust gene expression pattern in response to changing environment. DNA-dependent RNA polymerase (RNAP), 1 which is composed of an essential catalytic core enzyme (␣ 2 ␤␤Ј ) and one of the sigma ( ) factors, is the central enzyme for expression of genomic information in all organisms.Rifampicin (Rif) inhibits transcription initiation by blocking the ␤ subunit of bacterial RNAP (1, 2). Many Rif-resistant (Rif r ) mutants have been isolated and characterized in various bacteria, notably Escherichia coli. To our knowledge, most Rif r mutations are found within the rpoB gene that encodes the ␤ subunit of RNAP (3-6). E. coli Rif r rpoB mutations that suppress the auxotrophy due to lack of stringent response were demonstrated to affect the transcription of stringently controlled genes by destabilizing the RNAP-stable RNA promoter complex (7). Recently, we successfully activated the secondary metabolism (antibiotic production) by introducing certain Rif r rpoB mutations in Streptomyces coelicolor A3(2) and Streptomyces lividans (8 -11). On the basis of those findings, we proposed that improvement of RNAP by introduction of a Rif r mutation can be useful to elicit bacterial ability by altering the gene expression in a variety of microorganisms.The members of the genus Bacillus produce several antibiotics to inhibit growth of the competing organisms in nature. Neotrehalosadiamine (3,3Ј-diamino-3,3Ј-dideoxy-␣,␤-trehalose; NTD), which is an aminosugar antibiotic produced by Bacillus pumilus (12) and Bacillus circulans (13), inhibits growth of Staphylococcus a...

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“…Both SMC and MukB were shown to cooperate with two accessory proteins, which regulate their function [Hirano and Hirano, 2004] and are essential for their activity in vivo [Yamanaka et al, 1996;Mascarenhas et al, 2002]. Inactivation of either of these complexes leads to temperaturesensitive growth due to a severe disturbance of nucleoid organization and chromosome segregation at elevated temperatures [Niki et al, 1991;Britton et al, 1998;Moriya et al, 1998;Jensen and Shapiro, 1999]. This phenotype was shown to be suppressed by mutations that cause excessive negative supercoiling, which suggests a role for these proteins in DNA compaction or folding [Sawitzke and Austin, 2000;Lindow et al, 2002a].…”

Section: Mechansims Of Nucleoid Organizationmentioning

confidence: 99%

The bacterial nucleoid: A highly organized and dynamic structure

Thanbichler

Wang

Shapiro

2005

J of Cellular Biochemistry

122

101

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Recent advances in bacterial cell biology have revealed unanticipated structural and functional complexity, reminiscent of eukaryotic cells. Particular progress has been made in understanding the structure, replication, and segregation of the bacterial chromosome. It emerged that multiple mechanisms cooperate to establish a dynamic assembly of supercoiled domains, which are stacked in consecutive order to adopt a defined higher-level organization. The position of genetic loci on the chromosome is thereby linearly correlated with their position in the cell. SMC complexes and histone-like proteins continuously remodel the nucleoid to reconcile chromatin compaction with DNA replication and gene regulation. Moreover, active transport processes ensure the efficient segregation of sister chromosomes and the faithful restoration of nucleoid organization while DNA replication and condensation are in progress.

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A Bacillus subtilis gene‐encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition

Cited by 178 publications

References 44 publications

Penicillin-Binding Protein-Related Factor A Is Required for Proper Chromosome Segregation in Bacillus subtilis

Penicillin-Binding Protein-Related Factor A Is Required for Proper Chromosome Segregation in Bacillus subtilis

RNA Polymerase Mutation Activates the Production of a Dormant Antibiotic 3,3′-Neotrehalosadiamine via an Autoinduction Mechanism in Bacillus subtilis

The bacterial nucleoid: A highly organized and dynamic structure

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