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Chapter 9 : Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination

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Abstract:

This chapter reviews briefly the properties of integrons and gene cassettes, and provides a mechanistic framework for integron-mediated gene cassette mobility using the typical tyrosine recombinase mechanism as a perspective. The tyrosine recombinase family is characterized both by the conservation of key catalytic residues and a shared mechanism of recombination. The most common and widely studied type of integron, the type 1 integron (sometimes referred to as the class 1 integron), encodes the IntI1 recombinase and contains the recombination site. Gene cassettes usually include a single gene with very little extraneous noncoding DNA. Cassettes are usually integrated in only one of the two possible orientations within an integron, that orientation allowing for the expression of genes from P. This orientation specificity appears to be determined by polarity within the recombination sites, which determines how they align and recombine. Integron-mediated gene cassette mobilization is the most promiscuous site-specific recombination system known. An enormous range of specific recombination sites of different sequences, including hundreds of cassette-associated sites, at least four sites, and potentially hundreds of secondary sites, are recognized by at least four recombinase proteins. The similarity of integron-encoded recombinases with XerCD is interesting because XerCD seems to be good at stalling reaction at the Holliday junction (HJ) intermediate stage and at dealing with central region heterology. As almost all bacteria with circular chromosomes possess XerCD homologs, we speculate that IntI genes of integrons may have evolved from XerCD-encoding genes.

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9

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Ribosome Binding Site
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Genetic Elements
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Figures

Image of Figure 1.
Figure 1.

The integron-gene cassette site-specific recombination system. The recombination site into which cassettes are integrated is represented by a filled box, whereas the site of the gene cassette is shown as an open box. The gene encoding a tyrosine recombinase is transcribed by the promoter P, while promoter P directs transcription of integrated gene cassettes. Phenotypic markers are designated orf1 and orf2. A schematic model for the successive integration of two circular cassettes into the site of an integron is shown. Incoming cassettes are preferentially integrated at the site ( ).

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9
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Image of Figure 2.
Figure 2.

(A) Schematic representation of reactions catalyzed by tyrosine recombinases. Two recombinase molecules (ovals) are bound to each core recombination site. Recombination core sites synapse in an antiparallel orientation. In the first pair of strand exchanges two active recombinase monomers (unshaded) catalyze strand breakage and rejoining reactions of the thicker strands to generate a 2-fold symmetrical HJ intermediate, which then undergoes a conformational change to form a substrate for the second pair of strand exchanges. Tyrosine recombinases act on the “crossing” strands, the more acute pair of strands within the HJ. During the second pair of strand exchanges, the shaded recombinase monomers are active and catalyze breakage-rejoining of the thinner strands to generate recombinant products. (B) Structure of representative core recombination sites (not to scale). The site is recognized by the phage P1 encoded Cre protein, the site by Flp encoded by the yeast 2μm plasmid, the site by XerCD, and the site by λ Int. Recombinase binding sites are represented by shaded horizontal arrows separated by a central region of 6 to 8 bp. The positions of strand exchange at each end of the central region are indicated by vertical arrows. Additional recombinase binding sites and binding sites for accessory proteins are also indicated.

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9
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Image of Figure 3.
Figure 3.

Sequences of integron-encoded recombinases. (A) Alignment of four characterized IntI proteins. Conserved amino acid residues are shown below the alignment. The conserved catalytic RKHRHY residues of tyrosine recombinases and type IB topoisomerases are shaded. The horizontal line above the IntI1 sequence indicates that region shown in panel B. Sequences are derived from NCBI entries AAB59081 (IntI1), L10818 (IntI2), BAA08929 (IntI3), and AAD53319 (IntI, previously IntI4). The complete IntI2 sequence is obtained by removing an internal premature termination codon at position 179. (B) A conserved IntI-specific motif. Alignment of sequences from integron recombinases (highlighted in panel A) with corresponding regions of five other representative tyrosine recombinases: XerD from (P21891), TnpI from Tn(P10020), TnpI from Tn(AAA64588), phage λ Int (P03700), and the phage P1 encoded Cre (CAA27178). Amino acids completely conserved in IntI proteins but absent from other tyrosine recombinases (Holmes, personal communication) are shaded. This integron recombinase-specific motif lies at a position equivalent to that between α-helices I and J of XerD ( ). (C) Comparisons of recombinase sequences derived from sequence alignment in reference . Conserved residues are shaded. The sequences shown correspond to part of the conserved motif III of Xer recombinases which contains the catalytic lysine that is present in all tyrosine recombinases and type IB topoisomerases ( ).

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9
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Image of Figure 5.
Figure 5.

(A) Comparison of site organization in related systems. Recombination site features are depicted as in Fig. 4 . The relative orientations of the respective recombinase genes are shown. The Tnrecombination site organization is derived from information in reference . Note that, based on analogy to characterized systems, the central region in this site is assumed to be 6 bp. The Tn recombination site organization is derived from reference and V. Vanhooff and B. Hallet (personal communication). The length of central region in this site has been determined experimentally (Vanhooff and Hallet, personal communication). The uncharacterized recombination site found in a putative transposon from ( ) was determined from analysis of the sequence in GenBank database entry U14952. (B) Comparison of the sequences immediately adjacent to the central regions (and hence strand cleavage positions) in the recombination sites shown in panel A with those of sites recognized by the XerC and XerD recombinases (//) ( ). The central regions of each site are AT rich. A conserved consensus for the presumptive complete 11-bp IntI recombinase binding sites in and is presented and compared with the remarkably similar sequence bound by XerD. The consensus is derived from the information in Fig. 4 .

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9
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Image of Figure 4.
Figure 4.

Recombination site organization. (A) Sequence of the site (from type 1 integrons) required for efficient in vivo recombination. The 7-bp conserved sequence at the right end is shown in bold. The location of the normal recombination crossover position within this conserved sequence is marked by a thick vertical arrow. The thin vertical arrow indicates the location of recombination crossover events identified in rare recombinants and defines the second recombinase-mediated cleavage site. The extent of protected regions in methylation interference assays ( ) is indicated by horizontal lines, corresponding to regions DR1 and DR2 and containing directly repeated accessory recombinase binding sites that contain the consensus DNA binding sequence ( Fig. 5 ). The regions marked L and R represent recombinase binding sites within the core recombination site. Below the sequence is a schematic representation of site organization. Recombinase binding sites are shown as shaded arrows. The number indicates the length of the predicted central region between inversely oriented IntI binding sites. The orientation of the gene is also shown. Note that recombinase-mediated cleavage is presumed to occur on the strands and positions indicated by vertical arrows by analogy to the characterized tyrosine recombination systems and the known strand cleavage positions, 3′ of an A residue, in Xer recombination ( ). (B) site organization. Sequence of the sequence. The 7-bp inverted repeat conserved sequences found at each end are shown in bold. A major recombination crossover position is indicated by a thick vertical arrow. Alternative crossover positions in rare recombinants are indicated by thin vertical arrows. Sequences conserved between more than 60 sequences and representing the inner portion of putative IntI binding sites ( ) are shaded. Invariably, the DNA sequence between L′ and L″ shows inverted repeat character. A schematic representation of organization is shown below. The break between L′ and L″ indicates that the length of this sequence can be longer than that of the sequence shown here. Features are as in panel A. (C) Comparison of four known sequences. Regions of extensive conservation are highlighted, with recombinase binding sites indicated by underlining. A schematic of the proposed recombinase binding sites is shown below. CR indicates the central region. Sequences are derived from database entries referred to in Fig. 3A . Features are as in panel A.

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9
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Tables

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Table 1

IntI1-catalyzed recombination events

Citation: Recchia G, Sherratt D. 2002. Gene Acquisition in Bacteria by Integron-Mediated Site-Specific Recombination, p 162-176. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch9

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