Structure and regulation of the dnaA promoter region in three Streptomyces species

Jakimowicz, Dagmara; Majka, Jerzy; Lis, Bartłomiej; Konopa, Grażyna; Węgrzyn, Grzegorz; Messer, Walter; Schrempf, Hildgund; Zakrzewska‐Czerwińska, Jolanta

doi:10.1007/pl00008652

Cited by 16 publications

(15 citation statements)

References 32 publications

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“…However, only the dnaA-dnaN region was required to achieve a functional origin when subcloned onto a plasmid, although the rpmH-dnaA DnaA-box clusters did have an effect on origin replication. As before, dnaA transcription was autoregulated by binding of DnaA to DnaA-box clusters in the dnaA promoter (28).…”

Section: Oric Architecturesupporting

confidence: 58%

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

2012

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bMuch of our knowledge of the initiation of DNA replication comes from studies in the Gram-negative model organism Escherichia coli. However, the location and structure of the origin of replication within the E. coli genome and the identification and study of the proteins which constitute the E. coli initiation complex suggest that it might not be as universal as once thought. The archetypal low-G؉C-content Gram-positive Firmicutes initiate DNA replication via a unique primosomal machinery, quite distinct from that seen in E. coli, and an examination of oriC in the Firmicutes species Bacillus subtilis indicates that it might provide a better model for the ancestral bacterial origin of replication. Therefore, the study of replication initiation in organisms other than E. coli, such as B. subtilis, will greatly advance our knowledge and understanding of these processes as a whole. In this minireview, we highlight the structure-function relationships of the Firmicutes primosomal proteins, discuss the significance of their oriC architecture, and present a model for replication initiation at oriC. The Firmicutes are Gram-positive bacteria encompassing three major classes, Bacilli, Clostridia, and Mollicutes. They have a relatively low GϩC content in their genomes and are morphologically and physiologically diverse. Rod-shaped bacilli, spherical cocci, and aerobic, anaerobic spore-forming, and non-sporeforming bacteria are found in this group. They likely represent the most ancestral phylum of prokaryotes, with high-GϩC-content Gram-positive and Gram-negative bacteria having diverged from the Firmicutes at a later stage in evolution (13,70). Bacillus subtilis is the best studied of the Firmicutes and is widely considered the Gram-positive model bacterium, but other bacilli, streptococci, staphylococci, and clostridia have been extensively studied because of their medical and industrial importance.In addition to the universally conserved replication initiation protein DnaA (32, 65) and the replication restart protein PriA (17, 39), the low-GϩC-content Firmicutes generally have two unique essential genes, dnaD and dnaB, coding for the replication initiation proteins DnaD and DnaB, respectively ( Table 1) (note that DnaB in B. subtilis is unrelated to DnaB in Escherichia coli). In some cases-for example, in several Mollicutes-there are no distinct dnaD and dnaB genes, but there is, instead, a single gene annotated as dnaD-like which may combine both functions. No homologous proteins are found outside the Firmicutes, suggesting a replication initiation machinery distinctly different from those of other bacteria (31). In addition, there are a number of regulatory proteins which are not found in the Gram-negative model organism Escherichia coli, including YabA, Soj, SirA, and Spo0A, while other regulatory proteins are found in E. coli but not B. subtilis (these regulatory proteins have been subject to a recent review [29]). DnaA, DnaD, and DnaB, together with the helicase loader DnaI (called DnaC in E. coli), the replicativ...

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Section: Oric Architecturesupporting

confidence: 58%

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

2012

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“…Thus, the DnaA boxes might serve as regulatory elements. Indeed, the two boxes in the dnaA promoter are bound by DnaA, and the expression of dnaA is autoregulated (19). In addition, we identified clusters of DnaA boxes containing five or six DnaA boxes within a relatively short distance (213 to 329 bp) (Fig.…”

Section: Resultsmentioning

confidence: 82%

“…Interestingly, most of the strong DnaA boxes (42 of 51) lie in noncoding DNA regions upstream of genes. In many cases a single strong DnaA box is present in a putative promoter region, and sometimes a strong box is accompanied by a weak one, as illustrated by the promoter region of dnaA itself (19,36). Thus, the DnaA boxes might serve as regulatory elements.…”

Section: Resultsmentioning

confidence: 99%

Cluster of DnaA Boxes Involved in Regulation of Streptomyces Chromosome Replication: from In Silico to In Vivo Studies

et al. 2006

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In Streptomyces coelicolor, replication is initiated by the DnaA protein in the centrally located oriC region and proceeds bidirectionally until the replication forks reach the ends of the linear chromosome. We identified three clusters of DnaA boxes (H69, H24, and D78) which are in a relatively short segment of the chromosome centered on the oriC region. Of the clusters analyzed, D78 exhibited the highest affinity for the DnaA protein; the affinity of DnaA for the D78 cluster was about eightfold higher than the affinity for oriC. The high-affinity DnaA boxes appear to be involved in the control of chromosome replication. Deletion of D78 resulted in more frequent chromosome replication (an elevated ratio of origins to chromosome ends was observed) and activated aerial mycelium formation, leading to earlier colony maturation. In contrast, extra copies of D78 (delivered on a plasmid) caused slow colony growth, presumably because of a reduction in the frequency of initiation of chromosome replication. This suggests that the number of high-affinity DnaA boxes is relatively constant in hyphal compartments and that deletion of D78 therefore permits an increased copy number of either the chromosomal origin region or a plasmid harboring the D78 cluster. This system conceivably influences the timing of decisions to initiate aerial mycelial formation and sporulation.

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“…The initiator protein DnaA of Streptomyces contains two dimerization domains (I and III) that are separated by a long flexible domain II. According to our preliminary results (16,22), interaction of the DnaA protein with two DnaA boxes exhibits cooperativity (e.g. the DnaA protein specifically binds to DNA fragments with two "weak" DnaA boxes, which are not bound as individ- The Streptomyces DnaA Protein Prefers the E. coli DnaA Box over Its Own DnaA Box-Analysis of 57 DnaA boxes from three different Streptomyces oriC regions showed that the preferred sequence is 5Ј-TTGTCCACA-3Ј ("strong" DnaA box).…”

Section: Discussionmentioning

confidence: 99%

Sequence Recognition, Cooperative Interaction, and Dimerization of the Initiator Protein DnaA of Streptomyces

Majka

Zakrzewska‐Czerwińska

Messer

2001

Journal of Biological Chemistry

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Using a combined PCR-gel retardation assay, the preferred recognition sequence of the Streptomyces initiator protein DnaA was determined. The protein showed a preference toward DNA containing two Escherichia coli-like DnaA boxes in a head-to-head arrangement (consensus sequence TTATCCACA, whereas the consensus sequence of the DnaA boxes found in the Streptomyces oriC region is TTGTCCACA). In quantitative band shift experiments, the kinetics of the Streptomyces DnaADnaA box interaction was characterized. The DnaA protein can form dimers while binding to a single DnaA box; dimer formation is mediated by the domain III of the protein, and the dissociation constant of this process was between 35 and 115 nM. Streptomyces initiator protein DnaA interacts in a cooperative manner with DNA containing multiple binding sites. For the cooperativity effect, which seems to be independent of the distance separating the DnaA boxes, domain I (or I and II) is responsible. The cooperativity constant is moderate and is in the range of 20 -110.

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Structure and regulation of the dnaA promoter region in three Streptomyces species

Cited by 16 publications

References 32 publications

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

Chromosomal Replication Initiation Machinery of Low-G+C-Content Firmicutes

Cluster of DnaA Boxes Involved in Regulation of Streptomyces Chromosome Replication: from In Silico to In Vivo Studies

Sequence Recognition, Cooperative Interaction, and Dimerization of the Initiator Protein DnaA of Streptomyces

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