Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC

Katayama, Tsutomu; Ozaki, Shogo; Keyamura, Kenji; Fujimitsu, Kazuyuki

doi:10.1038/nrmicro2314

Cited by 267 publications

(400 citation statements)

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“…DnaA binds to the DnaA box located at oriC to facilitate the unwinding of duplex strands (Katayama et al, 2010;Scholefield et al, 2011); consequently, replisome complexes are recruited to the unwinded oriC. As such, DnaA is essential for DNA replication initiation in most bacteria.…”

Section: Introductionmentioning

confidence: 99%

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

et al. 2015

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Regulating DNA replication is essential for all living cells. The DNA replication initiation factor DnaA is highly conserved in prokaryotes and is required for accurate initiation of chromosomal replication at oriC. DnaA-independent free-living bacteria have not been identified. The dnaA gene is absent in plastids and some symbiotic bacteria, although it is not known when or how DnaA-independent mechanisms were acquired. Here, we show that the degree of dependency of DNA replication on DnaA varies among cyanobacterial species. Deletion of the dnaA gene in Synechococcus elongatus PCC 7942 shifted DNA replication from oriC to a different site as a result of the integration of an episomal plasmid. Moreover, viability during the stationary phase was higher in dnaA disruptants than in wild-type cells. Deletion of dnaA did not affect DNA replication or cell growth in Synechocystis sp. PCC 6803 or Anabaena sp. PCC 7120, indicating that functional dependency on DnaA was already lost in some nonsymbiotic cyanobacterial lineages during diversification. Therefore, we proposed that cyanobacteria acquired DnaA-independent replication mechanisms before symbiosis and such an ancestral cyanobacterium was the sole primary endosymbiont to form a plastid precursor.

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Section: Introductionmentioning

confidence: 99%

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

et al. 2015

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“…In the initiation complex of bacterial genome replication, multiple molecules of DnaA bind to oriC via its domain IV and form a helical shape through homooligomerization of DnaA's domain III (1)(2)(3)(4)(5). Despite the fact that high-resolution structures have previously been solved for DnaA, the entire complex structure remains to be explored.…”

Section: Discussionmentioning

confidence: 99%

“…In a model organism, Escherichia coli, DnaA forms homooligomers on the replication origin oriC, which promotes dsDNA unwinding. The resulting ssDNA is captured by DnaB helicase, followed by formation of the replisomes (2)(3)(4)(5). Molecular mechanisms of how DnaA facilitates dsDNA unwinding are still unclear, although some models have been proposed (1,(6)(7)(8)(9)(10).…”

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“…A crystal structure model is available for the complex of domain IV with dsDNA for E. coli DnaA (21). Domain III is the multifunctional ATPases associated with various cellular activities (AAA+) domain, which tightly binds ATP and ADP (1)(2)(3)(4)(5)(23)(24)(25). The ATP-bound AAA+ domain can form stable helical homooligomers by assembling in a head-to-tail manner (Fig.…”

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“…1A) (1)(2)(3)(4)(5)(11)(12)(13)(14)(15). The DnaA boxes contain 9-mer nucleotides (consensus sequence TTATNCACA, where N can be any base) (16).…”

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Near-Atomic Structural Model for Bacterial DNA Replication Initiation Complex and its Functional Insights

Shimizu

Noguchi

Sakiyama

et al. 2017

Biophysical Journal

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Upon DNA replication initiation in Escherichia coli, the initiator protein DnaA forms higher-order complexes with the chromosomal origin oriC and a DNA-bending protein IHF. Although tertiary structures of DnaA and IHF have previously been elucidated, dynamic structures of oriC-DnaA-IHF complexes remain unknown. Here, combining computer simulations with biochemical assays, we obtained models at almost-atomic resolution for the central part of the oriC-DnaA-IHF complex. This complex can be divided into three subcomplexes; the left and right subcomplexes include pentameric DnaA bound in a head-to-tail manner and the middle subcomplex contains only a single DnaA. In the left and right subcomplexes, DnaA ATPases associated with various cellular activities (AAA+) domain III formed helices with specific structural differences in interdomain orientations, provoking a bend in the bound DNA. In the left subcomplex a continuous DnaA chain exists, including insertion of IHF into the DNA looping, consistent with the DNA unwinding function of the complex. The intervening spaces in those subcomplexes are crucial for DNA unwinding and loading of DnaB helicases. Taken together, this model provides a reasonable near-atomic level structural solution of the initiation complex, including the dynamic conformations and spatial arrangements of DnaA subcomplexes.DnaA | molecular simulation | coarse-grained model | oriC C hromosomal DNA replication is initiated by unwinding the dsDNA of the replication origin, which requires formation of higher-order protein-DNA complexes, typically referred to as the initiation complexes (1). DnaA is a major replication initiation protein conserved in the initiation complex of most eubacterial species. In a model organism, Escherichia coli, DnaA forms homooligomers on the replication origin oriC, which promotes dsDNA unwinding. The resulting ssDNA is captured by DnaB helicase, followed by formation of the replisomes (2-5). Molecular mechanisms of how DnaA facilitates dsDNA unwinding are still unclear, although some models have been proposed (1, 6-10). A high-resolution structure model of the initiation complex, discovered using computational modeling based on experimental data, would provide significant insight into the molecular mechanism.The E. coli minimal oriC region contains the AT-rich DNA unwinding element (DUE), at least 11 DnaA-binding motifs (termed DnaA boxes) and a single binding site for the integration host factor (IHF) (Fig. 1A) (1-5, 11-15). The DnaA boxes contain 9-mer nucleotides (consensus sequence TTATNCACA, where N can be any base) (16). The 11 DnaA boxes (R1-2, R4, R5M, I1-3, C1-3, and τ2) have differing affinities to DnaA and motif orientations (indicated by triangles in Fig. 1A): The two terminal boxes R1 and R4 have especially high affinities (dissociation constants 1-6 nM for R1 and ∼1 nM for R4), whereas others have modest (R2) to low affinities (I1-3, C1-3, and R5M and τ2; dissociation constants for R5M are >200 nM) (12-19). The 11 DnaA boxes have been divided into two groups...

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Binary Fission in Bacteria

Margolin¹

2014

Encyclopedia of Life Sciences

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Given a suitable environment, most free‐living prokaryotic cells (including bacteria) will grow continually until, on reaching a critical size, they divide into two equal‐sized parts in a process called binary fission. To be successful, this process requires the accurate duplication and partition of the chromosomes, and subsequent splitting of the cytoplasm precisely at the cell midpoint. The latter process, known as cytokinesis, often uses a large transmembrane protein machine that includes homologues of actin and tubulin as well as enzymes that synthesise and degrade specific portions of the cell wall. The placement of this machine is often regulated by negatively acting morphogen gradients. Once assembled, numerous accessory proteins respond to various inputs to regulate how and when the machine constricts and cells physically separate. Key Concepts: The timing of chromosome duplication in bacteria responds to cell growth rate and initiates at a specific location only once per cell cycle. Bacterial chromosomes are organised and condensed by DNA‐binding proteins, some of which are conserved from bacteria to humans. Bacterial cells use homologues of eukaryotic cytoskeletal proteins actin and tubulin to organise their growth and division. Morphogen gradients of negative spatial regulators help to position the cytokinetic ring in many bacteria. Recent advances in synthetic biology of bacterial cytokinesis are increasing our understanding of key components.

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Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC

Cited by 267 publications

References 103 publications

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

Diversification of DnaA dependency for DNA replication in cyanobacterial evolution

Near-Atomic Structural Model for Bacterial DNA Replication Initiation Complex and its Functional Insights

Binary Fission in Bacteria

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