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Chapter 8 : Illegitimate Recombination in Bacteria

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Abstract:

Illegitimate recombination is a ubiquitous phenomenon and includes three types of events. In the first class, rearrangements occur by recombination between short homologous sequences. A second class is associated with site-specific elements. A last class groups all rearrangements in which the newly linked sequences share less than 3 bp of homology and have no homology with known specific sites. Oxidative lesions are known to induce rearrangements. Deletions by illegitimate recombination between short homologous sequences were reported in mutants, in which a defect in iron metabolism regulation results in increased oxidative damage. In bacteria, transcription inhibits deletion between tandemly repeated sequences 10-fold. In contrast, transcription was shown to increase recombination between nonhomologous sequence. The stimulation of transposon excision by rolling-circle replication adds to the long list of indirect evidence that supports the occurrence of the replication slippage events in vivo. Most of the genetic studies of illegitimate recombination were performed in , either on the chromosome or with bacteriophages. Most of the recombination events between short homologous sequences occur independently from the action of RecA, since the length considered is far below the minimum efficient processing segment (MEPS). Topoisomerases are enzymes that modify the supercoiling of molecules through transient breakage and ligation of DNA strands. The first evidence that topoisomerases may promote rearrangements in bacteria came from the work of Ikeda and collaborators. Illegitimate recombination is a major issue in eukaryotes, because it is at the origin of numerous pathological disorders.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8

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Type II Topoisomerase
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Replication Fork
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Type I Topoisomerase
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Figures

Image of FIGURE 1
FIGURE 1

Model of deletion by replication slippage between two short homologous sequences. The directly repeated (DR) sequences are indicated by shaded boxes and the arrows above the boxes. The hatched lines represent newly synthesized DNA strands, and a, b, and с are the DNA regions flanking (a and c) and between (b) the repeated sequences. A pause of the DNA polymerase during the synthesis of the first DR encountered allows the opening of the DNA. Erroneous pairing with the other DR leads to the loss of the b region and of one of the repeated sequences. The deletion is stabilized by replication continuation. Duplication of the b sequence and of one of the DR occurs when DNA synthesis pauses at the second DR encountered and the newly synthesized DNA folds back, allowing erroneous pairing with the first DR and a second replication of the b region (not shown).

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 2
FIGURE 2

Model of deletion between two short homologous sequences by SSA. The directly repeated (DR) sequences are indicated by grey boxes and the arrows above the boxes. The initiating event is a DNA DSB occurring between the repeated sequences. Exonucleolytic degradation of one of the strands renders short homologous sequences single stranded, which allows them to pair. Degradation by exonucleases of the single-stranded tails, gap filling by a polymerase, and ligation lead to the deletion of the b region (defined in the legend to Fig. 1 ) and of one DR.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 3
FIGURE 3

Repair of a broken replication fork by SSA (reproduced from reference ). A replication fork arrested at a (T) site is represented. Short repeated sequences (1 and 2) are shown as bold lines. (a) Breakage of the lagging-strand template in the vicinity of , generating a DSB. (b) Nucleolytic degradation of the exposed 5′ ends, generating a 3′-tailed single-stranded region, (c) Annealing of complementary sequences 1 and 2. (d) The intermediate is repaired by removal of the 3′ tail, gap filling, and ligation. A round of replication produces the deletant plasmid molecule. Arrows indicate the 3′ ends of leading and lagging strands.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 4
FIGURE 4

Model of SbcCD action (reproduced, with permission, from reference ). During the replication of a palindromic sequence, intrastrand base pairing can cause pausing of DNA replication and is a potential precursor for deletion. To reinitiate replication, the SbcCD protein removes the secondary structure and generates a DSB. This DSB is repaired by homologous recombination with the sister chromosome to allow the reconstitution of a replication fork. This model specifically predicts that the intact copy of the palindromic sequence is replicated again after reconstitution of the replication fork.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 5
FIGURE 5

Schematic model of deletion formation by one-ended transposition. The transposon is shown as a shaded box; the bound transposase is shown as an oval. One end of the transposon and the target (T) are acted upon by the transposase. The region (b) between the transposon end and the target is excised by the transposase and deleted. Regions a and с are the regions flanking the deleted sequences.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 6
FIGURE 6

Model for deletion formation by erroneous action of gyrase. Gyrase is shown as two rectangles, corresponding to the two subunits of the enzyme. Gyrase binds to double-stranded DNA and introduces a double-strand cut. Exchange of subunits between two gyrase molecules, acting at different places on a DNA molecule or on two different DNA molecules, and resealing by gyrase lead to rearrangement. Bold and thin lines are two different DNA molecules. White and gray rectangles are two different gyrase molecules.

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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Image of FIGURE 7
FIGURE 7

Models for TopA-mediated deletion formation between divergent replication forks blocked at sites (reproduced from reference ). The 1- 2 replication intermediate is partially represented; template strands are shown as thin lines, and newly synthesized leading and lagging strands are shown as continuous and interrupted thick arrows, respectively. О and T represent and replication terminators, respectively. The 5′ and 3′ ends generated by topoisomerase cleavage are represented by a point and a thin arrow, respectively. Deletion can result either from the junction of the template strands (model A) or from the junction of the newly synthesized strands (model B). In model A, topoisomerase-mediated cleavage occurs at each of the two replication forks, in the vicinity of sites (A1); a topoisomerase molecule (a) covalently linked to the 5′ end generated on the leading-strand template catalyzes by error ligation with the 3′ end created by another topoisomerase molecule (b) at the other replication fork (A2); this leads to the excision of a gap-containing molecule, which is converted into a circular double-stranded plasmid by continuation of leading-strand synthesis (A3). In model B, a topoisomerase molecule cleaves the lagging strand in the vicinity of a site (B1); this molecule, bound to the 5′ end, catalyzes the joining to the 3′ end of the leading strand at the other blocked replication fork (B2); a circular double-stranded deletant plasmid is generated by another round of replication (B3).

Citation: Michel B. 1999. Illegitimate Recombination in Bacteria, p 129-150. In Charlebois R (ed), Organization of the Prokaryotic Genome. ASM Press, Washington, DC. doi: 10.1128/9781555818180.ch8
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