Termination of DNA Replication in Prokaryotes


Most bacteria and archaea have circular chromosomes, in which DNA replication begins at a site known as an origin of replication. Double‐stranded DNA unwound at the origin creates two replication forks that are engaged by DNA polymerase complexes (replisomes) that advance each fork and proceed in opposite directions away from the origin, copying the original strands. Termination of DNA replication occurs when the two forks meet and fuse, creating two separate double‐stranded DNA molecules. In the well‐studied bacteria Escherichia coli and Bacillus subtilis, this occurs in the terminus region, which is situated diametrically opposite the origin. Failure to terminate chromosome replication correctly can lead to problems with genome function and stability, including DNA over‐replication. In contrast, some archaea have multi‐origin chromosomes and do not appear to specifically regulate the location of termination.

Key Concepts

  • Termination of DNA replication occurs when two oppositely orientated replication forks meet and fuse, to create two separate and complete double‐stranded DNA molecules.
  • In circular bacterial chromosomes, termination is restricted to a region called the terminus region, located approximately opposite the origin of replication.
  • A replication fork trap is an opposing arrangement of unidirectional replication terminator (Ter) sites in a region of DNA, which allows replication forks to enter the trap from either direction, but not exit it.
  • Failure to terminate bacterial chromosome replication correctly results in chromosome over‐replication and genome instability.
  • Terminator proteins bind to asymmetric DNA Ter sites to arrest a replication fork approaching the non‐permissive side but allow fork passage from permissive side.

Keywords: DNA replication; replication termination; replication fork arrest; DNA terminators; replication terminator protein; termination utilisation substance; catenanes

Figure 1. Arrangement ofDNAreplication terminators in the circular chromosomes of (a)Escherichia coliand (c)Bacillus subtilis. The two replication forks generated at the origin (oriC) move in opposite directions along the DNA and eventually approach one other and fuse within the terminus region diametrically opposed to oriC. The terminus region constitutes a replication fork trap in which the DNA terminators (denoted Ter) are arranged as two opposed groups, with the red terminators oriented to block movement of the clockwise replication fork and the blue terminators oriented to block the anticlockwise fork. Letters and Roman numbers define Ter sites (A indicates the location of TerA in E. coli; I indicates the location of TerI in B. subtilis). The STer region of the B. subtilis chromosome contains additional terminator sites used only during the stringent response. The chromosomal locations for the origin, the dif chromosome dimer resolution site and the genes for the terminator proteins, Tus (terminus utilisation substance) in E. coli and RTP (replication terminator protein) in B. subtilis, are marked. The location of rrn operons, which are highly transcribed particularly under fast growth conditions, are shown by green arrows, with the arrow pointing in the direction in which transcribing RNA polymerase molecules travel. (b) & (d) show consensus sequences for the E. coli Ter core sequence and the B. subtilis terminators. For B. subtilis the overlapping A and B sites are indicated.
Figure 2. Crystal structures of Terminator protein‐DNAcomplexes. (a) Two crystal structures of the Tus–Ter complex of E. coli indicating the blocking and permissive ends of the complex (left, PDB 2i05), and in the ‘locked’ conformation with DNA unwound at the blocking end and the C6 base of Ter DNA bound to its specific binding pocket in Tus (right, PDB 2i06), which contributes significantly to the fork arrest activity of the complex. (b) Crystal structure of an RTP dimer in complex with the high‐affinity half of TerI (the B site) (PDB 2efw). RTP can form a symmetric dimer in solution and recognises the partial DNA sequence symmetry in each half‐site that makes up each functional Ter site in B. subtilis. However, the partial asymmetry of each half‐site causes the RTP monomers to adopt somewhat different conformations in the half‐site complex (‘wing‐up’ conformation, on the left‐hand monomer, and ‘wing‐down’ conformation on the right‐hand monomer as viewed), and this might play a specific role in establishing cooperativity of binding to the second low‐affinity half‐site (the A site), and optimising contact with the oncoming replisome for its arrest. The cooperative binding of two dimers to each Ter site is essential for fork arrest activity. In the full complex, forks would be arrested when approaching from the right in the image shown. The structural basis for cooperative binding and how the whole complex interacts with the replisome are unknown features of interest.
Figure 3. Chromosome replication and cell growth in cells with one or two replication origins in the presence and absence of a replication fork trap. (a) In the presence of a block to one replication fork on its way from oriC to the termination area the chromosome will remain under‐replicated, as the second fork will be blocked by the Ter/Tus complexes in the termination area. (b) Schematic representation of the replichore arrangement of an E. coli chromosome with an ectopic replication origin termed oriZ in the presence of a functional replication fork trap. oriZ indicates the integration of a duplication of the oriC sequence near the lacZYA operon (Wang et al., ). Directionality of replication and fork fusion locations are indicated by green arrows. (c) Replichore parameters in the termination area of E. coli cells with two replication origins in the absence of a functional replication fork trap (Δtus). If forks escaping the termination area proceed with a speed similar to forks coming from oriC, then the fusion point should be in the location indicated by the blue arrows. If forks escaping the termination area are slowed by an increased number of replication–transcription conflicts, then forks should fuse closer to the termination area, as indicated by the grey arrows. The experimental observation is, however, that the fork fusion point is located closer to oriC (green arrows), indicating that forks escaping the termination area potentially encounter fewer problems than forks coming from oriC (Ivanova et al., ). (d) Schematic representation of the replichore arrangement of an E. coli chromosome replicating exclusively from an ectopic replication origin in the presence (d i) and absence (d ii) of a functional replication fork trap. Directionality of replication and approximate fork fusion locations are indicated by green and blue arrows in the presence and absence of a functional fork trap (Δtus), respectively.
Figure 4. Over‐replication in the termination area in the absence ofRecGhelicase (a) Replication profiles of E. coli cells in exponential phase. The number of reads (normalised against the reads for a stationary wild‐type control) is plotted against the chromosomal coordinate. Positions of oriC (green line) and primary Ter sites are shown above the plotted data with red and blue lines representing the left and right replichore as depicted in a. The termination area between the innermost Ter sites is highlighted in light blue. (b) Growth of a ΔrecG Δtus rpo* strain in which the entire oriC region is deleted. (c) Marker frequency analysis of a ΔrecG Δtus rpo* strain that carries a temperature‐sensitive allele of the main replication initiator protein DnaA. The strain was grown at 42 °C to inactivate DnaA(ts) and therefore prevent n from being active. (d) Marker frequency analysis of chromosome replication in a double origin strain in the presence and absence of RecG. Strains were grown at 37 °C. Reproduced with permission from Rudolph et al. 2013. © Nature.
Figure 5. Schematic illustrating how replication fork fusions might trigger over‐replication in the termination area and how this is normally prevented by proteins such as RecG and/or 3′ exonucleases. Note that the formation of a 3′ flap can occur at both forks. However, for simplicity, the schematic shows only one such reaction. See text for further details.


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Rudolph, Christian J, Corocher, Tayla‐Ann, Grainge, Ian, and Duggin, Iain G(Jan 2019) Termination of DNA Replication in Prokaryotes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001056.pub3]