Chapter 34 : Mariner and the ITm Superfamily of Transposons

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The mariner elements belong to the ITm superfamily of cut-and-paste DNA-transposons. The acronym is derived from the IS630, Tc1, and mariner elements, which represent three major divisions within the grouping. The first member of the superfamily to be documented was Tc1 in in 1983 ( ). A few years later, Mos1 and IS630 were identified in and the bacterium , respectively ( ). A steady stream of ITm elements entered the literature in subsequent years. However, these were the tip of an iceberg and the depth and breadth of their phylogenetic distribution did not start to become apparent until 1993 when PCR experiments using mariner-specific primers revealed their presence in seven orders of insects ( ). We now know that ITm is probably the most widespread superfamily of transposons in nature and that they are present in all branches of the tree of life ( Fig. 1 ) ( ).

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Image of Figure 1
Figure 1

Taxonomic distribution of DNA transposons across the eukaryotic tree of life. Five eukaryotic super-groups are indicated with thickened lines. Asterisks indicate the numbers of genomes representing the branch: *, 1 genome; **, 2 to 5 genomes; ***, 6 to 10 genomes; ****, over 10 genomes. Figure reproduced from ( ) with permission of the authors and the publisher.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 2

Organization of ITm transposons and mariner transposases. (A) ITm transposons are ∼1.5 to 2.5 kb in length. In Tc3 and SB, ITRs have two transposase binding sites. In mariner, ITRs are ∼30 bp and carry a single transposase binding site. ITm transposons have a single ORF, which codes for the transposase and is rarely interrupted by an intron. (B) Mariner transposases have an N-terminal DNA-binding domain with two helix-turn-helix (HTH) motifs and a C-terminal catalytic domain with three aspartate (D) residues that coordinate the catalytic metal ions. The DNA-binding and catalytic domains are joined by a linker region that includes the highly conserved stretch of amino acids, WVPHEL. YSPDL is another highly conserved motif that occurs just before the third aspartate. Both conserved motifs are important in communication between the active sites (see text for details).

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 3

Phylogeny of the ITm transposons. ITm families are classified according to their triad of catalytic residues and the number of amino acids separating the second aspartate (D) and the third aspartate or glutamate (E). Sequences of the catalytic domains for 15 ITm transposases were extracted from Repbase, aligned with MUSCLE, and an unrooted tree was constructed with Mega 6.06 using HIV integrase as an outgroup.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 4

Nucleotidyl transfer reactions catalyzed by RNase-H type enzymes. (A) Double strand cleavage at the ends of mariner transposons. The first nick is usually recessed three nucleotides within the transposon DNA and exposes a 5′-phosphate on the end of the transposon. The second nick is precisely at the transposon end and exposes the 3′-hydroxyl, which is subsequently transferred to the target. (B) RNase H hydrolyzes the RNA strand in an RNA–DNA hybrid. (C) The transition state in the two metal-ion mechanism for nucleotidyl transfer reactions is illustrated. The RNase-H fold coordinates two divalent metal ions via three (or four) acidic residues. The figure illustrates the metal binding pocket of Hsmar1, which has three conserved aspartate (D) residues. The proposed transition state is shown with the nucleophile, R–O attacking from the right in an in-line configuration with the leaving group (the 3′-OH of the transposon). Several different nucleophiles, including HO and glycerol, can be used in strand cleavage. The proposed role of the DDD triad in coordinating a pair of divalent metal ions and their role as Lewis acids and bases in promoting the reaction are indicated. (D) Several mechanisms of strand cleavage and joining reactions and the role of divalent metal ions in transposition are illustrated. DNA transposons can be classified according to the sequence of hydrolysis and transesterification reactions. Metal ions are designed H or T to indicate their role in activating the nucleophile in hydrolysis and transesterification reactions, respectively (see text for details). In the H–T–T mechanism illustrated for the hAT transposons (center) we have assumed that the reaction is performed by a single active site. If this is the case, the active site would have to be reorganized to capture the 3′-end of the transposon in preparation for the integration step. This is illustrated as a 180° rotation of the transposon end and the active site with respect to each other. If the mariner elements are also cleaved by a single active site a reorganization would be required between the two hydrolysis steps to exchange the top and bottom strands in the active site. See text for further details.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 5

Models for the mechanism of mariner transposition. (A) Three proposed models for the arrangement of subunits in mariner cleavage: (1) tetramer; (2) subunit exchange; and (3) dimer models. Single-end complex 2 (SEC2) contains a transposase dimer and one transposon end. Paired-ends complex (PEC) contains two transposon ends and two or four subunits. The open and filled circles represent the DNA strand containing the 5′- and 3′-ends of the transposon, respectively, viewed down the axis of the double helix. (B) The nucleoprotein complexes deduced from biochemical analysis of Hsmar1 transposition are illustrated using the dimer model for cleavage. Binding of a transposase dimer to the first transposon end is fast. Recruitment of the second end within SEC2 is slow. Catalysis is within the context of the PEC. The 5′ strands of the transposon ends are cleaved first, followed by a structural change that is coordinated between ends. This is followed by cleavage of the 3′-ends and transposon integration.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 6

Autoregulation of mariner transposition by OPI. (A) Model of the ASO mechanism that underlies OPI in mariner transposition. PEC assembly is by recruitment of a naked transposon end. As the concentration of transposase rises, naked ends are sequestered leading to inhibition of the reaction. (B) Simulation of a genomic invasion by a mariner transposon. If the affinity of the transposase dimer for the first and second transposon ends are the same, OPI only starts to reduce the rate of transposition once there are a very large number of transposons contributing to the pool of transposase. The timescale of the simulation is very short because transposition events in the computer model are allowed to yield products instantly and the low rate of diffusion , owing to molecular crowding, has been ignored. See text for further details. (C) Simulation as in part (B) except that we account for allosterism, which slows synapsis by reducing the affinity of the developing transpososome for the second transposon end compared to the first. Part (B) reproduced from ( ) available under Creative Commons License.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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Figure 7

Structural features of mariner transposition intermediates. (A) A cartoon illustrating the -architecture of the Mos1 transpososome as visualized in the crystal structure of the postcleavage intermediate ( ). Green and orange blobs, transposase; blue, active site; green, clamp loop; red, WVPHEL motif; purple, YSPDL motif. (B, C) Cartoon and space filling representation for the interactions between the clamp loop and the WVPHEL motif at the dimer interface. Coordinates from PDB HOT3. (D to F) The relationship between the catalytic domain of protein subunits in the crystal structures of the Mos1 PEC (PDB HOT3), the Mos1 catalytic domain (PDB 2F7T), and the SETMAR catalytic domain (PDB 3K9J). The three beta sheets forming the core of the RNase H fold are shown together with the third conserved aspartate residue from the active site. (G) One of the structural elements from the dimer interface in SETMAR (PDB 3K9J) is shown, highlighting residue R141 (numbering from Hsmar1). (H) A cartoon illustrating the elongation of the transposase dimer during first end binding as suggested by neutron scattering experiments. Part (A) reproduced from ( ) available under Creative Commons License. Parts (B) and (C) reproduced from ( ) available under Creative Commons License. Part (H) reproduced from ( ) available under Creative Commons License.

Citation: Tellier M, Bouuaert C, Chalmers R. 2015. Mariner and the ITm Superfamily of Transposons, p 753-772. 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.MDNA3-0033-2014
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