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Chapter 28 : The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism

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Abstract:

Members of the widespread IS/IS bacterial insertion sequence (IS) family transpose using obligatory single-strand (ss) DNA intermediates. This distinguishes them from classical IS, which move via double-strand (ds) DNA intermediates (see Siguier et al., this volume). Members of this family also differ fundamentally from classic IS in their organization. They carry subterminal palindromic structures instead of inverted repeats at their ends ( Figure 1A ) and insert 3′ to specific AT-rich tetra- or penta-nucleotides without duplicating the target site. Importantly, the transposase, TnpA, does not share characteristics of the “DDE” enzymes of classical IS. It is a member of the “HuH” superfamily of enzymes including relaxases, Rep proteins of rolling circle replication (RCR) plasmids/single-stranded phages, bacterial and eukaryotic transposases of IS/IS, and helitrons (see Thomas and Pritham, this volume) ( ), which all catalyze cleavage and rejoining of ssDNA substrates. IS, the founding member, was identified 30 years ago in ( ) but there has been renewed interest for these elements since the identification of the IS group in ( ). Studies of two elements of this group, IS from and IS from the radiation-resistant , have provided a detailed picture of their mobility ( ).

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014

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Figures

Image of Figure 1
Figure 1

Organization of IS/IS family. (A) Genetic organization. Left (LE) and right (RE) ends carrying the subterminal hairpin (HP) are presented as red and blue boxes, respectively (colour code retained throughout). Left and right cleavage sites (C and C) are presented as black and blue boxes respectively, where the black box also represents element-specific tetra-/pentanucleotide target site (T). The cleavage positions are indicated by small vertical arrows. Gray arrows: and open reading frames (s); (i) IS group with alone; (ii) to (iv) IS group with and in different configurations; (v) IS group with alone. (B) IS. Secondary structures in the LE, adapted from reference : promoter (p), ribosome binding site (RBS), start and stop codons (AUG and UAA) are indicated. (i) DNA top strand with perfect palindromes at LE and RE in red and blue, interior stem–loop in black, (ii) RNA stem–loop structure in transcript originated from p. (C) Organization of TnpB protein and derivatives: putative N-terminal helix-turn-helix motif (HTH), central OrfB_IS domain with a putative DDE motif (Pfam) and C-terminal zinc finger motif (ZF) are shown. Numbers represent occurrence of corresponding variants among 85 analyzed sequences: 46 carry all the three domains (e.g., IS), 33 lack HTH motif (e.g., IS), whereas others retain separate domains. doi:10.1128/microbiolspec.MDNA3-0039-2014.f1

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 2
Figure 2

IS and transposition cycle. IS organization. The left (LE) and right (RE) ends with subterminal hairpin (HP) are in red and blue, left and right cleavage sites (C/T and C) are represented by black and blue boxes, respectively. Excision. (A) TnpA activity: top strand (active strand) structures are recognized and cleaved by TnpA (vertical arrows). (B) Upon cleavage, a 5′ phosphotyrosine bond (green cylinder) is formed with LE and with the RE 3′ flank and 3′-OH (yellow circle) is formed at left flank and RE. (C) Excision of the IS single-strand circle intermediate with abutted LE and RE (RE–LE junction or transposon joint) (C) accompanied by formation of donor joint retaining the target sequence. (D) The transposase catalyzes the cleavage of transposon joint and single-strand target (E) then integration (F). doi:10.1128/microbiolspec.MDNA3-0039-2014.f2

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 3
Figure 3

TnpA structures (adapted from references and ). (A) Crystallographic structure of TnpA alone. The two monomers of the TnpA dimer are colored green and orange, respectively. Positions of helix αD and catalytic residues are shown. (B) Costructure TnpA–RE HP22. HP22 is shown in blue. The extrahelical T17 and the T located in the hairpin loop are indicated in red ( ). Note that in the TnpA–HP22 costructure, binding sites for the hairpins are located on the same face of the TnpA dimer whereas the two catalytic sites are formed on the opposite surface (A, C–F). (C) Configuration of the active site in the TnpA–RE HP22. HP22 is shown in blue. Note that in A, B and C, TnpA is in the inactive conformation. The arrow shows the presumed rotation of the αD helix to activate the protein. (D) Configuration of the active site in the TnpA–LE HP26 costructure. LE HP26 is shown in red and the 5′ 4-nucleotide extension (G) in yellow). The base A+18 has displaced Y127 to activate the protein. (E) TnpA–RE35 complex. Interaction of G-C (in light and dark blue, respectively) positions the cleavage site within the catalytic site of the protein. (F) Modeled TnpA–LE–RE complex. LE, RE, and flanking sequences in red, blue, and black, respectively. doi:10.1128/microbiolspec.MDNA3-0039-2014.f3

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 4a
Figure 4a

Recognition of cleavage sites. Schematic of the canonical and noncanonical base interactions in (A) left end (LE) and (B) right end (RE). The LE and RE are shown in red and blue. Cleavage sequences C or C are placed in black or dark blue boxes; guide sequences G and G are framed in pink and light blue, respectively. Two nucleotides at the 3′ foot of HP involved in triplet formation are highlighted by bold and in black frame. Nucleotide sequences of LE and RE and the base paring within HP and HP are shown. The inset figures describe the interactions between the cleavage sequences and guide sequences. The filled lines indicate canonical base interactions and the dotted lines indicate additional noncanonical base interactions. (C) Structure of the co-complex TnpA–RE35 adapted from reference showing the active site and the base pairs between C (TCAA, dark blue) and G (GAAT, light blue). The gray sphere is bound Mn. Right: Two base triplets observed in the TnpA–RE35 complex. (D) Target recognition: single-strand transposon joint (RE–LE junction) and target Ts are presented. For simplicity only the recognition of the target cleavage site is indicated. (E) Cleavage sites recognition in the IS/IS family. Multiple sequence alignment of the cleavage sites and guide sequences using Weblogo (weblogo.berkeley.edu) was carried out on 38, 43 and 23 members of the IS (i), the IS (ii), and the IS (iii) groups, respectively. (F) Linker length distribution of LE and RE from 76 (red) and 80 (blue) different IS, respectively. doi:10.1128/microbiolspec.MDNA3-0039-2014.f4a

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 4b
Figure 4b

Recognition of cleavage sites. Schematic of the canonical and noncanonical base interactions in (A) left end (LE) and (B) right end (RE). The LE and RE are shown in red and blue. Cleavage sequences C or C are placed in black or dark blue boxes; guide sequences G and G are framed in pink and light blue, respectively. Two nucleotides at the 3′ foot of HP involved in triplet formation are highlighted by bold and in black frame. Nucleotide sequences of LE and RE and the base paring within HP and HP are shown. The inset figures describe the interactions between the cleavage sequences and guide sequences. The filled lines indicate canonical base interactions and the dotted lines indicate additional noncanonical base interactions. (C) Structure of the co-complex TnpA–RE35 adapted from reference showing the active site and the base pairs between C (TCAA, dark blue) and G (GAAT, light blue). The gray sphere is bound Mn. Right: Two base triplets observed in the TnpA–RE35 complex. (D) Target recognition: single-strand transposon joint (RE–LE junction) and target Ts are presented. For simplicity only the recognition of the target cleavage site is indicated. (E) Cleavage sites recognition in the IS/IS family. Multiple sequence alignment of the cleavage sites and guide sequences using Weblogo (weblogo.berkeley.edu) was carried out on 38, 43 and 23 members of the IS (i), the IS (ii), and the IS (iii) groups, respectively. (F) Linker length distribution of LE and RE from 76 (red) and 80 (blue) different IS, respectively. doi:10.1128/microbiolspec.MDNA3-0039-2014.f4b

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 5
Figure 5

Strand transfer and reset model of IS transpososome. (A) Inactive form of TnpA dimer in the absence of DNA (pale green, orange ovals and dark green and orange cylinders represent the body and the αD helices of two monomers, respectively). At the ends, dotted red and blue lines represent linkers at left end (LE) and right end (RE), light red and light blue boxes represent G and G, respectively. (B) Binding of a copy of LE and RE resulting in TnpA activation (catalytic sites ). (C) Cleavage of both ends forms a 5′ phosphotyrosine linkage between Y127 and LE on one αD helix (dark orange cylinders) and between Y127 and the RE flank on the other (dark green cylinders). 3′-OH groups are shown as yellow circles. Reciprocal rotation of both αD helices from to configuration are indicated by large arrows. (D) Strand transfer takes place to reconstitute the joined donor backbone (donor joint) and generate the RE–LE transposon junction at configuration. (E) Release of the donor joint and transition from to configuration. (F) Reset to the form and target site engagement. (G) Cleavage of the RE–LE junction and target and transition from to configuration. (H) Regeneration of the left and right transposon ends. doi:10.1128/microbiolspec.MDNA3-0039-2014.f5

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 6
Figure 6

Transposition of the IS/IS family and the replication fork: “Peel and Paste” transposition mechanism. (A) Excision. Cartoon representing excision of the single-strand circular intermediate (transposon joint) from the lagging strand template of a donor plasmid. Arrow tip represents replication direction. (B) Integration. Integration of right end (RE)–left end (LE) transposon joint into single-strand target at the replication fork. doi:10.1128/microbiolspec.MDNA3-0039-2014.f6

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 7a
Figure 7a

Y1 transposase domestication. (A) repeated extragenic palindromes (REP), bacterial interspersed mosaic elements (BIME) and REPtron. (i) Representation of two categories of REP structures in / with mismatches in the hairpin stem in orange and light blue, violet box represents the conserved tetranucleotide GTAG. Corresponding iREP structures in red and dark blue where green box represents the complementary tetranucleotide CTAC. (ii) Structure of BIME: REP and iREP separated by linkers C or D. BIME are frequently found as consecutive copies. (iii) Examples of REPtrons from some representative strains. is shown in gray, the flanking genes and in green and in violet, respectively. Arrows represent the direction of transcription. (B) IStron: organization of IStron where Intron and IS parts are indicated. P1–P8 and IGS represents characteristic features of group I Introns. LE, RE, TTGAT target site and two of the IS part are indicated. doi:10.1128/microbiolspec.MDNA3-0039-2014.f7a

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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Image of Figure 7b
Figure 7b

Y1 transposase domestication. (A) repeated extragenic palindromes (REP), bacterial interspersed mosaic elements (BIME) and REPtron. (i) Representation of two categories of REP structures in / with mismatches in the hairpin stem in orange and light blue, violet box represents the conserved tetranucleotide GTAG. Corresponding iREP structures in red and dark blue where green box represents the complementary tetranucleotide CTAC. (ii) Structure of BIME: REP and iREP separated by linkers C or D. BIME are frequently found as consecutive copies. (iii) Examples of REPtrons from some representative strains. is shown in gray, the flanking genes and in green and in violet, respectively. Arrows represent the direction of transcription. (B) IStron: organization of IStron where Intron and IS parts are indicated. P1–P8 and IGS represents characteristic features of group I Introns. LE, RE, TTGAT target site and two of the IS part are indicated. doi:10.1128/microbiolspec.MDNA3-0039-2014.f7b

Citation: He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B. 2015. The IS/IS Family and “Peel and Paste” Single-strand Transposition Mechanism, p 609-630. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0039-2014
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