oriC-encoded instructions for the initiation of bacterial chromosome replication

Abstract

Replication of the bacterial chromosome initiates at a single origin of replication that is called oriC. This occurs via the concerted action of numerous proteins, including DnaA, which acts as an initiator. The origin sequences vary across species, but all bacterial oriCs contain the information necessary to guide assembly of the DnaA protein complex at oriC, triggering the unwinding of DNA and the beginning of replication. The requisite information is encoded in the unique arrangement of specific sequences called DnaA boxes, which form a framework for DnaA binding and assembly. Other crucial sequences of bacterial origin include DNA unwinding element (DUE, which designates the site at which oriC melts under the influence of DnaA) and binding sites for additional proteins that positively or negatively regulate the initiation process. In this review, we summarize our current knowledge and understanding of the information encoded in bacterial origins of chromosomal replication, particularly in the context of replication initiation and its regulation. We show that oriC encoded instructions allow not only for initiation but also for precise regulation of replication initiation and coordination of chromosomal replication with the cell cycle (also in response to environmental signals). We focus on Escherichia coli, and then expand our discussion to include several other microorganisms in which additional regulatory proteins have been recently shown to be involved in coordinating replication initiation to other cellular processes (e.g., Bacillus, Caulobacter, Helicobacter, Mycobacterium, and Streptomyces). We discuss diversity of bacterial oriC regions with the main focus on roles of individual DNA recognition sequences at oriC in binding the initiator and regulatory proteins as well as the overall impact of these proteins on the formation of initiation complex.

Protein-induced DNA linking number change by sequence-specific DNA binding proteins and its biological effects

“…Transcription/promoters are also found near bacterial DNA replication origins (Leonard and Grimwade 2015;Wolanski et al 2014). In many cases, promoters direct transcription away from DUE of bacterial origins (Leonard and Grimwade 2015;Wolanski et al 2014). It is possible that transcription-coupled DNA supercoiling greatly facilitates opening/melting DUE of bacterial replication origins.…”

“…Specifically, the BO-some^(26) functioning as a DNA topological barrier (Leng et al 2011) blocks, confines, and captures transcription-coupled DNA supercoiling, which unwinds DUE of Oriλ (30) and initiates DNA replication (Chung 1996). Transcription/promoters are also found near bacterial DNA replication origins (Leonard and Grimwade 2015;Wolanski et al 2014). In many cases, promoters direct transcription away from DUE of bacterial origins (Leonard and Grimwade 2015;Wolanski et al 2014).…”

“…As discussed above, DnaA and λ O utilize the protein-induced ΔLk to open/melt the AT-rich DUE of replication origins to initiate DNA replication Grimwade 2009, 2015;Magnan and Bates 2015;Rajewska et al 2012;Wolanski et al 2014). Additionally, the nucleoprotein complexes by these replication initiators functioning as a DNA topological barrier (Leng et al 2004(Leng et al , 2011Leng and McMacken 2002) block, confine, and capture transcription-coupled DNA supercoiling, which helps open/melt DUE of replication origins and facilitates DNA replication initiation (Chung 1996).…”

Identification and Characterization of Replication Origins of Multiple Chromosomes in Rhodobacter sphaeroides

“…As genes located in the oriC region are conserved across closely related bacterial species [21], the conserve gene-cluster within the known replication-origin regions can be utilized to predict putative origins of replication in related species, as shown in Figure 4 and Figure 5. For instance, comparison of the genome sequences of C. crescentus and R. prowazekii reveals that both species share a conserved gene-cluster near the established replication origins in C. crescentus and R. prowazekii [22][23][24].…”

Protein-induced DNA linking number change by sequence-specific DNA binding proteins and its biological effects

“…In bacteria, DNA replication usually initiates from a defined single site on the chromosome; the origin of DNA replication (OriC; Leonard and Grimwade 2009;Leonard and Grimwade 2015;Magnan and Bates 2015;Rajewska et al 2012;Wolanski et al 2014). OriC is composed of an AT-rich DNA unwinding element (DUE) and binding sites for DnaA or DnaA-like proteins (Leonard and Grimwade 2015;Rajewska et al 2012;Wolanski et al 2014).…”