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Chapter 26 : DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements

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Abstract:

This chapter talks about four different families of transposable DNA elements and describes how transposon-mediated recombination molds the organization of the bacterial chromosome. The four families were divided based on the proteins they encode for their mobility: (i) the DDE transposons, which include the majority of the classical bacterial elements such as IS3, IS50 (Tn5), IS10 (Tn10), Tn3, and phage Mu; (ii) the rolling circle transposons, called Y2-transposons and include IS91; (iii) the Y-transposons, which include the conjugative transposon Tn916; and (iv) the Stransposons, a newly recognized family that includes IS1535, IS607, and themobilizable transposon Tn4451. The mechanisms of transposition for each of these four families are very different, although the end products may often look quite similar. Their features were summarized in order to illustrate the different ways a transposon can move from one site to another and the different types of chromosomal rearrangement they can create. It is thought that immunity plays a key role in protecting a transposon from the damaging effects of its own transposition. Immunity in Tn7 parallels that of Mu, with TnsB and TnsC playing the roles of MuA and MuB. The author has compared and contrasted four families of transposable elements found in bacteria. Each family has developed distinct ways of translocating defined segments of DNA, although there are some unifying themes and many of the end products look identical.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26

Key Concept Ranking

Mobile Genetic Elements
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Long Terminal Repeat Retrotransposons
0.4365542
0.49051538
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Figures

Image of Figure 1.
Figure 1.

Comparison of the mechanisms of transposition utilized by the four transposon families. The figure highlights the major differences between transposition pathways; for specific details, see the text, Table 1, and Fig. 3 , Fig. 7 , Fig. 9 , and Fig. 10 . Heavy bar, transposon DNA; thin line, flanking donor DNA; thick line, target DNA; vertical arrows, sites of target cleavage; dashed bar, newly replicated DNA; boxed arrowhead, target duplication; circled Y or S, covalent phosphotyrosine or phosphoserine linkages of recombinase to DNA; open circles, exposed 3′-OH nucleophile. The fate of the donor DNA is not fully determined for nonreplicative transposition and is indicated by a question mark. Major differences to note are initial strand-cleavage events, transposase-DNA covalent linkages, role of DNA replication, circular intermediates, target-site duplications, and fate of the donor DNA.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 2.
Figure 2.

Intermolecular transposition can result in a simple insertion or a cointegrate, irrespective of the transposition pathway. Shown vertically are the expected transposition products for cut-and-paste and replicative integration. Each results in a target duplication, but only the replicative pathway duplicates the transposon and fuses the donor and target replicons. The question mark in the upper product for cut-and-paste transposition indicates that the fate of the donor DNA is unclear; the double-strand gap may be repaired, or the DNA may be degraded (see text and Fig. 6d for more details). Cointegrates can be reduced to form the target with a simple insertion and the initial donor, either by site-specific resolution or by homologous recombination between each transposon copy. Homologous recombination between donor and simple insertion product can also generate cointegrates. Dimerization of the donor plasmid followed by cut-and-paste transposition of the two transposons and intervening donor DNA (a composite transposon) will also result in a cointegrate. Symbols are as described in the legend to Fig. 1 .

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 3.
Figure 3.

Comparison of DDE transposition mechanisms (see text for details). Although, for simplicity, transposons are represented as straight lines, all transposase-mediated processes occur within a complex of two transposon ends and transposase. Cleavage at the ends of Tn7 (but not of the other elements shown) also requires the presence of the target DNA. Symbols are as described in Fig. 1. A and B for the Tn7 pathway indicate the TnsA and TnsB proteins required for cleavage at the 5′ and 3′ ends of the transposon, respectively; black triangles indicate the sites of transposase-mediated hydrolysis; scissile phosphates (P in a circle) are the sites of concerted cleavage and strand joining by the indicated 3′-OH nucleophile (connecting arrows). Note that for IS transposition, the initial strand-transfer event generates a figure-eight molecule, which is probably resolved by replication (not shown) to regenerate the parent molecule and a transposon circle with left and right ends separated by a few nucleotides. Nicking at each transposon end then linearizes the transposon circle. Adapted from reference 69.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 6.
Figure 6.

Intramolecular transposition. The figure shows how nonreplicative (a and b) and IS-like (c) elements can generate adjacent deletions and inversions even though each forms an excised, linear transposon intermediate. In each case, transposition involves a composite transposon, or ends from two transposons in the sister chromosome pathway (b). Note that duplicative inversion, as shown in panel b, is not associated with any DNA loss, in contrast to deletion-inversions (a and c). Cut-and-paste transposons can also transpose to intramolecular targets if transposition is associated with replication (d). The fate of the donor is unclear (indicated by brackets). The chromosome may be degraded, or it may be rescued by gap repair using the sister chromosome as a template.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 4.
Figure 4.

Switching from cut-and-paste transposition to replicative integration by Tn7 and IS903. Transposition of both elements is consistent with efficient cleavage of the 5′ ends of the transposon to generate an excised transposon (shown on the left), which is then integrated to form a simple insertion. TnsA mutants (B and A) of Tn7 fail to cleave at the 5′ ends of Tn7 and form strand-transfer intermediates. Mutations in IS903 located either at the transposon termini (IR) or close to the transposase active site (Tnp) result in elevated levels of cointegrate formation consistent with formation of the strand-transfer intermediate.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 5.
Figure 5.

Intramolecular transposition by elements that integrate replicatively generates adjacent deletions or adjacent inversions. The outcome of this event is determined simply by transposon-target strand connections. Symbols are as for Fig. 1. A, B, C, and D are four hypothetical genes used to depict the inversion event.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 7.
Figure 7.

Two models for rolling circle transposition. Left, the model of Mendiola et al. ( ); right, the model of Tavakoli et al. ( ). See the text for details. The Y2-transposase, which binds to the end of the transposon, cleaves 3′ to the sequence GTTC. is the second site of transposase cleavage and defines the 3′ end of the ssDNA form of the transposon.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 8.
Figure 8.

The ends of Tn, showing binding sites for the transposition proteins. The heavy line is Tn; the thin lines are the flanking DNA. Binding sites for the two domains of Int (the Y-transposase) are shown as arrowheads: black and white indicate sites for the C-terminal catalytic domain (the white arrowheads are the variable sites acquired from each target DNA); gray indicates sites for the N-terminal arm-site binding domain. Barred arrows indicate the Xis binding sites.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 9.
Figure 9.

Mechanism of Y-transposon excision. The heavy lines are the transposon ends, and the thin lines are the flanking donor DNA. The dashed portions represent the coupling sequences—the 6-bp duplex segment between the cleavage sites. Y, the free tyrosine nucleophiles; Y-, the covalent tyrosine-DNA linkages; O, free 5′ OHs positioned to attack the phosphotyrosine covalent linkages. Curved arrows show the nucleophilic attack of the YOH on the DNA cleavage site. The shaded asymmetric shapes represent the Y-transposase; dark subunits are in the active conformation, light subunits are inactive. Note the switch of both subunit activities and DNA conformations at the isomerization step. Transposon insertion involves synapsis of an excised transposon and a target site and occurs by reversal of the entire process. Adapted from reference .

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Image of Figure 10.
Figure 10.

Mechanism of S-transposon excision. The heavy lines are the transposon ends, and the thin lines are the flanking donor DNA. The cartoon shows the two DNA duplexes separated by a tetramer of S-transposase catalytic domains, as proposed in a recent model for synapsis by Aresolvase ( ). The shaded subunits are bound to the junction at the transposon's right end. Sthe free serine nucleophiles; S-, the covalent serine-DNA linkages; O, free 3′ OHs. Curved arrows show the coordinated nucleophilic attacks of SOH on the DNA cleavage sites (top panel) or 3′ OHs on the phosphoserines (third panel). Note that in this model, strand switching is accompanied by switching of the recombinase catalytic domains, since the two are covalently linked. Transposon insertion involves synapsis of an excised transposon and a target site, and occurs by reversal of the entire process. For further details, see the text.

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
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Tables

Generic image for table
Table 1.

Distinguishing characteristics of the four transposon families

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
Generic image for table
Table 2.

Comparison of the intramolecular products generated by the transposon families

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
Generic image for table
Table 3.

A sampling of Y-transposons

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26
Generic image for table
Table 4.

A sampling of S-transposons

Citation: Derbyshire K, Grindley N. 2005. DNA Transposons: Different Proteins and Mechanisms but Similar Rearrangements, p 467-497. In Higgins N (ed), The Bacterial Chromosome. ASM Press, Washington, DC. doi: 10.1128/9781555817640.ch26

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