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Chapter 29 : Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles

Authors: George Chaconas1, Carton W. Chen2
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Affiliations: 1: Department of Biochemistry and Molecular Biology and Department of Microbiology and Infectious Diseases, University of Calgary, Department of Biochemistry and Molecular Biology and Department of Microbiology and Infectious Diseases, University of Calgary; 2: Institute of Genetics, National Yang-Ming University, Shih-Pai, Taipei 112, Taiwan
Content Type: Monograph
Publication Year: 2005

Category: Microbial Genetics and Molecular Biology; Bacterial Pathogenesis

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Abstract:

This chapter focuses on the structure and associated functional features of the linear bacterial chromosomes of species and species. Telomere resolvases have also been referred to as protelomerases, for prokaryotic or proteic telomerases. Based upon the similarity of the telomeres on the chromosome to those on the linear plasmids, replication of the linear plasmids is also expected to be bidirectional from an internal origin. The recombination model suggests that homologous recombination would be essential for chromosomal replication and thus viability. Nevertheless, it is noteworthy that the recombination model in theory is blind to the sophisticated secondary structures at the 3’ overhangs during DNA replication. The chromosome sequence, however, contains an open reading frame encoding another α subunit of PolIII. There are also two copies of β and γ/τ subunits and three of ε subunits. The meaning of this multiplicity is not clear, but it is unlikely that an extra PolIII enzyme functions in terminal patching, because the DNA strand synthesized in terminal patching is expected to be relatively short , not necessitating the high processivity of such enzyme. The linear replicons of and , despite their identical topology, appear to be highly diversified in their structures and modes of replication. These two organisms use varied but highly effective mechanisms to ensure that the ends of their linear DNA molecules are faithfully replicated, thereby eliminating the need for circularity of their DNA.

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29

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Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles
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Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
/content/10.1128/9781555817640.chap29.fig29-1
Figure 1

Alignment of telomeres. The nucleotide sequences of the telomeres from linear replicons of the indicated species is shown ( ). Conserved telomeric regions are boxed and shaded. The question marks indicate that DNA sequencing around the hairpin was not performed, so there is some uncertainty as to the exact sequence of the turnaround.

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Figure 1

Alignment of telomeres. The nucleotide sequences of the telomeres from linear replicons of the indicated species is shown ( ). Conserved telomeric regions are boxed and shaded. The question marks indicate that DNA sequencing around the hairpin was not performed, so there is some uncertainty as to the exact sequence of the turnaround.

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
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Figure 2

The replication strategy for linear replicons with covalently closed hairpin ends in . The arrows labeled L and R indicate the inverted repeats at the left and right ends, respectively. The line bisecting the head-to-head (L′-L) and tail-to-tail (R-R′) telomere junctions in the replication intermediate is an axis of 180° rotational symmetry. The telomere breakage and reunion reaction is referred to as telomere resolution. Reprinted from reference with permission from Elsevier.

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Figure 2

The replication strategy for linear replicons with covalently closed hairpin ends in . The arrows labeled L and R indicate the inverted repeats at the left and right ends, respectively. The line bisecting the head-to-head (L′-L) and tail-to-tail (R-R′) telomere junctions in the replication intermediate is an axis of 180° rotational symmetry. The telomere breakage and reunion reaction is referred to as telomere resolution. Reprinted from reference with permission from Elsevier.

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
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Figure 3

Mechanism of action of ResT. (A) In a relaxed or linearized plasmid the telomere junction is presented as lineform DNA with a head-to-head structure for the inverted repeat (thin arrows). The scissile phosphates are noted with black dots and are 6 nucleotides apart on opposite strands, placing them on the same face of the DNA double helix. The shaded ovals represent ResT protomers, and the unshaded portions denote the active site with its putative tyrosine nucleophile (Y). The open arrows indicate the orientation of the ResT protomers. For simplicity, the reaction is drawn with active-site function in , although whether catalysis actually occurs in or in is not yet known. DNA cleavage is effected through nucleophilic attack by an active-site tyrosine residue which makes a covalent intermediate with the DNA through a 3′ phosphotyrosine linkage. The 5′ hydroxyl groups are brought into proximity with the phosphotyrosine linkage for transesterification by a conformational change in the complex or by simple dissociation, with joining of the bottom strand to the top strand to produce the DNA hairpin. (B) In a supercoiled plasmid the telomere junction is presented as cruciform DNA with the inverted repeats in the opposite orientation to that found in the lineform DNA. This structure would block interaction of ResT protomers by reversing their relative orientation. They would also be separated in space on the long arms of the extruded cruciform. Additionally, the cleavage sites are moved far from the strand to which they need to be joined for hairpin formation. Reprinted from reference with permission from Elsevier.

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Figure 3

Mechanism of action of ResT. (A) In a relaxed or linearized plasmid the telomere junction is presented as lineform DNA with a head-to-head structure for the inverted repeat (thin arrows). The scissile phosphates are noted with black dots and are 6 nucleotides apart on opposite strands, placing them on the same face of the DNA double helix. The shaded ovals represent ResT protomers, and the unshaded portions denote the active site with its putative tyrosine nucleophile (Y). The open arrows indicate the orientation of the ResT protomers. For simplicity, the reaction is drawn with active-site function in , although whether catalysis actually occurs in or in is not yet known. DNA cleavage is effected through nucleophilic attack by an active-site tyrosine residue which makes a covalent intermediate with the DNA through a 3′ phosphotyrosine linkage. The 5′ hydroxyl groups are brought into proximity with the phosphotyrosine linkage for transesterification by a conformational change in the complex or by simple dissociation, with joining of the bottom strand to the top strand to produce the DNA hairpin. (B) In a supercoiled plasmid the telomere junction is presented as cruciform DNA with the inverted repeats in the opposite orientation to that found in the lineform DNA. This structure would block interaction of ResT protomers by reversing their relative orientation. They would also be separated in space on the long arms of the extruded cruciform. Additionally, the cleavage sites are moved far from the strand to which they need to be joined for hairpin formation. Reprinted from reference with permission from Elsevier.

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
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Figure 4

Predicted secondary structure of the 3′ end of the chromosome. Roman numerals indicate palindrome numbers. The “rabbit ears” secondary structure of the terminal 119 nt based on autonomous parvovirus ( ) is included for comparison. The hairpin sequences that are homologous to a hairpin of the parvoviral genome are shaded. The putative Pu:Pu sheared pairings are indicated by black dots. Palindromes I′ to VII′ are conserved in most chromosomes. Palindromes VIII0 to X0 are absent from some. Modified from references and .

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Image of Figure 4
Figure 4

Predicted secondary structure of the 3′ end of the chromosome. Roman numerals indicate palindrome numbers. The “rabbit ears” secondary structure of the terminal 119 nt based on autonomous parvovirus ( ) is included for comparison. The hairpin sequences that are homologous to a hairpin of the parvoviral genome are shaded. The putative Pu:Pu sheared pairings are indicated by black dots. Palindromes I′ to VII′ are conserved in most chromosomes. Palindromes VIII0 to X0 are absent from some. Modified from references and .

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
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Figure 5

Four models for terminal patching of linear replicons. The intermediate telomere structure with the 3′ single-stranded overhang, which contains the conserved terminal palindromes (I′ to IV′ are indicated), is shown on the top. The terminal protein (TP) is indicated by the filled circle. New TP is represented by open circles, DNA polymerase is represented by open arrows, and newly synthesized DNA is represented by dashed lines. See the text for details about the models. Modified from reference .

10.1128/9781555817640/fig29-5_thmb.gif
10.1128/9781555817640/fig29-5.gif
Image of Figure 5
Figure 5

Four models for terminal patching of linear replicons. The intermediate telomere structure with the 3′ single-stranded overhang, which contains the conserved terminal palindromes (I′ to IV′ are indicated), is shown on the top. The terminal protein (TP) is indicated by the filled circle. New TP is represented by open circles, DNA polymerase is represented by open arrows, and newly synthesized DNA is represented by dashed lines. See the text for details about the models. Modified from reference .

Citation: Chaconas G, Chen C. 2005. Replication of Linear Bacterial Chromosomes: No Longer Going Around in Circles, p 525-540. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch29
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