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Chapter 13 : Linear Plasmids in Bacteria: Common Origins, Uncommon Ends

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Abstract:

This chapter reviews the structure and replication of bacterial linear plasmids. Examples are given of the varying structures of the termini (telomeres) of linear plasmids from representative bacteria, and proposed mechanisms for telomere replication and resolution are described. Although the focus is on linear plasmids, most of what is described in the chapter also applies to linear bacterial chromosomes. The first bacterial linear plasmid was described in 1979 from the antibiotic-producing soil microbe . A few species with linear plasmids or chromosomes have also been found in the alpha, beta, and gamma divisions of the genus . In bacteria with polyploid stages, such as the mycelium of , linear DNA may segregate with fewer mishaps than circular DNA. Alternatively, one could argue that conversion of a circular replicon to a linear form was an inadvertent but neutral event. Linear plasmids have also been identified in the actinomycetes , , , , , and the proteobacteria and . Linear plasmids generally retain the same features and mechanisms for replication initiation as their circular counterparts. Recent experiments demonstrate that replication initiates from an internal origin and continues around the hairpin telomeres, resulting in a circular dimer. The segregation systems of all linear plasmids characterized to date, regardless of telomere structure, appear to be analogous to those of circular plasmids.

Citation: Stewart P, Rosa P, Tilly K. 2004. Linear Plasmids in Bacteria: Common Origins, Uncommon Ends, p 291-301. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch13

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Figure 1

Distribution of linear DNA among phylogenetically diverse bacteria. The tree was derived from 16S rDNA sequences by Hugenholrz ( ) and modified with permission. Phyla are shown as wedges, with their widths representing the known degree of divergence within that phylum. Phyla with cultivated members are shown in black, whereas those known only from environmental sequences (named by a member within the group) are shown in white. Groups with known linear DNA are shown on the right, with the form of the DNA (when known or presumed) indicated. Bars with loops on either end indicate linear DNA with hairpin ends, and bars with stars on either end indicate protein-capped ends. Species in which the sole identified linear species is a phage genome have the phage name in parentheses after the species name. Linear DNA may be present but not yet detected in other groups of bacteria. References arc in the text. Scale bar = 0.1 changes per nucleotide.

Citation: Stewart P, Rosa P, Tilly K. 2004. Linear Plasmids in Bacteria: Common Origins, Uncommon Ends, p 291-301. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch13
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Image of Figure 2
Figure 2

Model for replication of linear plasmids with covalently closed hairpin ends. Replication initiates from an internal origin and proceeds bidirectionally, producing a circular dimer intermediate with joined telomeric sequences producing inverted repeats (arrows). The replicated telomere sequence serves as a recognition site for the telomere resolvase (insert symbol) , which cleaves both DNA strands and then joins opposite strands together to create two linear plasmids with covalently closed hairpin telomeres. This model has been more fully described by Casjens ( ).

Citation: Stewart P, Rosa P, Tilly K. 2004. Linear Plasmids in Bacteria: Common Origins, Uncommon Ends, p 291-301. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch13
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Image of Figure 3
Figure 3

Model for replication of linear plasmids with protein-capped ends. Bidirectional replication from an internal origin results in a gap at the 5 end of the newly synthesized strand when the RNA primer is removed. Two general models for filling the gaps are depicted and are based on models for the replication of the linear chromosome of spp. Inverted repeat sequences of the single-stranded 3′ overhang fold together to form stem-loop structures. (A) The terminal protein (?) recognizes the complex secondary structure of the 3 DNA strand and serves as a protein primer for DNA polymerase to initiate replication and fill the gap. B. The folded 3 terminus forms the double-stranded primer necessary for DNA polymerase to initiate replication and fill the gap. Subsequently, the terminal protein binds and nicks the DNA near the beginning of the inverted repeat regions. DNA polymerase then proceeds in a 5 to 3 direction from the original template strand and fills the remaining gap. Variations on these models have been proposed and are reviewed by Chaconas and Chen ( ).

Citation: Stewart P, Rosa P, Tilly K. 2004. Linear Plasmids in Bacteria: Common Origins, Uncommon Ends, p 291-301. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch13
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