Transposons: Prokaryotic

Abstract

Transposons are DNA (deoxyribonucleic acid) segments found ubiquitously in the genomes of living organisms and capable of moving from place to place within a genome. They are frequently associated with the sequestration and transmission of accessory genes in bacteria and archaea. They carry genes such as resistance to anti‐bacterials, virulence and symbiotic factors and catabolism of xenobiotics. They have a large impact on public health by facilitating the spread of these phenotypic characters. Transposons generate a variety of DNA rearrangements that have profound consequences for cell survival and evolution. These rearrangements are associated with transposition events (catalysed by transposon‐specific enzymes, transposases) but repeated transposon copies can act as portable regions of homology and undergo homologous recombination using the host recombination system. Transposons are diverse in structure, highly regulated by a multitude of mechanisms but only specify a limited number of catalytic chemistries. Transposons can represent a large proportion of prokaryotic genomes.

Key Concepts

  • Transposable elements are ubiquitous and show a high degree of diversity.
  • Transposable elements use a limited number of different chemical mechanisms for their transposition.
  • Transposons are key elements in the short‐term evolution of prokaryotic genomes.
  • Trasposons are central to driving the spread of antibiotic resistance.

Keywords: compound transposons; unit transposons; transposon groups; mechanism

Figure 1. Organisation of different types of transposable elements. The figure is not to scale. The TE is shown as a pink box; purple arrows, Tpase genes; red arrows and boxes, passenger genes; blue arrows, regulatory and conjugation genes; white arrows, hypothetical proteins, dark blue arrows, terminal inverted repeats; white asterisks, GATC Dam methylation sites; OE and IE, outside ends and inside ends of the IS with respect to the transposon. (a) Compound transposons. This is a generic cartoon showing the general arrangement of flanking IS in several different Tn. Tn5 (5818 bp) carries inverted copies of IS50 (1534 bp); Tn10 (9147 bp) carries inverted copies of IS10 (1329 bp); Tn903 (3094 bp) carries inverted copies of IS903 (1057 bp, Tpase 307 aa); Tn9 (2638 bp) carries direct flanking copies of IS1 (768bp); Tn602 (3064 bp) carries direct flanking copies of IS903. Tpase, Tpase; kan, tet, cam: resistance genes for kanamycin, tetracycline and chloramphenicol respectively. (b) The Tn3 transposon family. TnpA, Tn3 Tpase; blue boxes, res recombination site, yellow boxes, toxin/antitoxin genes; green arrow, resolvases; Tn3, S‐recombinase; Tn4430, Y‐recombinase; TnXax1, Y‐recombinase and helper protein; TnXc4, large S‐recombinase; Tn21, Y‐recombinase showing the embedded res site. The length of each Tn3 family example is indicated. (c) Tn7 family. A canonical Tn7 family transposon is shown. The series of blue arrows below indicate the arrangements of the Tpase (TnsB) binding sites at each end. (d) Transposable phage (Phafe Mu). The map of the bacteriophage Mu genome shows the phage regulatory genes MuC (the phage repressor) and ner, together with the Tpase, MuA and the accessory MuB protein. Expression of MuB is probably translationally coupled to that of MuA. The late genes include phage capsid protein. MuA binding sites at each end are indicated by blue arrows. (e) Relationship between IS, MITEs, tIS and MICs. The (hypothetical) relationship between different IS derivatives. Horizontal arrows indicate open reading frames encoding the Tpase and passenger genes. (f) ICE with Y‐ or S‐recombinases. The figure shows two closely related ICE that share their conjugation genes, their origins of transfer (red vertical arrowhead) and the tetracycline resistance gene tetM but differ in the type of ‘transposase’ they encode. Tn916 (18 032 bp) possesses a bacteriophage lambda‐like system including a tyrosine site‐specific recombinase (int) and a gene required with int for excision (xis). In Tn5397 (20 658 bp) the int/xis system is replaced by a site‐specific serine recombinase gene tndX. A group II intron insertion has occurred into one of the conjugation‐like genes in Tn5397. (g) ICE with DDE transposases. The relationship between two ICE from Streptococcus agalactiae and a simple insertion sequence, ISLre2 is shown. (h) IS91 and ISCR families. Flanking DNA (deoxyribonucleic acid) is shown in green. IS91 itself includes an additional gene (light blue arrow) of unknown function, which is not present in all members of the family. Subterminal secondary structures essential for transposition are shown as small dark triangles. These are known as Ori‐IS and ter‐IS involved with initiation and termination of transposition on the rolling circle transposition model. Other, serendipitous, ter sequences are shown as vertical dotted lines on the right of the transposon. These are used when ter‐IS fails and results in the frequent incorporation of flanking genes into the transposon. A canonical ISCR is also shown. The ori‐IS and ter‐IS sequences are less obvious in this class of element and resistance genes are observed both downstream and upstream.
Figure 2. Replicative transposition (DDE). The figure shows the transposition mechanism of replicative TE that use a DDE Tpase. All DDE‐catalysed reactions require a divalent metal cation such as Mg2+ as a cofactor. The transposon is represented as a pink line. Flanking sequences in the donor molecule are blue. Flanking sequences in the target molecule are green. Red circles indicate 3′OH moieties generated by Tpase‐catalysed hydrolysis. Red boxes indicate target DNA flanks that are duplicated on insertion. Left hand panel: transposition of TE such as Tn3 and bacteriophage Mu. Top to bottom: Tpase catalysed cleavage at the 3′ transposon ends using H2O as the nucleophile. Liberated 3′OH attack the target in a staggered manner to create a branched molecule in which the transposon bridges both donor and target molecules. Replication proceeds, probably using the 3′OH liberated in the flanking target DNA, to generate a second transposon copy (newly replicated DNA is shown as a dotted orange line). If donor and target DNA are circular molecules, this fuses the two resulting in a cointegrate where the donor and target DNA are joined at each junction by a TE copy. Recombination between the two directly repeated TE ‘resolves’ the cointegrate into the original donor molecule and a target that now contains a copy of the TE. Recombination may use the host homologous recombination system but in the case of the Tn3 family, TnpR, one of several alternative site‐specific recombinases, promotes recombination at a specific DNA sequence, the res site. Right hand panel: Many TE, primarily the IS, generate an excised transposon circle as a transposition intermediate. This occurs by Tpase‐catalysed hydrolysis at a single end. The resulting 3′OH then attacks the opposite TE end to make a single‐strand bridge creating a 3′OH on the flanking donor DNA. This is then used to prime replication of the TE generating an excised double‐strand circular TE copy and regenerating the donor molecule. Tpase then engages with the circle, and catalyses hydrolysis of each end, again generating a 3′OH, which then attacks the target DNA in a staggered manner.
Figure 3. Nonreplicative (conservative) transposition (DDE). DDE enzymes are involved in different types of nonreplicative (conservative) transposition. Left hand panel: Some TE are simply cleaved from their neighbouring donor DNA flanks. This can be achieved by two enzymes each specific for one strand as occurs in Tn7 with TnsA and TnsB. For others such as IS630 and the eukaryotic Tc elements an initial DDE catalysed cleavage occurs at the 5′ end of the element (sometimes a short distance within the transposon itself) prior to cleavage of the 3′OH. Right hand panel: Transposition of IS4 IS family members (IS10 and IS50) involves formation of a tight DNA hairpin at the TE ends. The DDE Tpase first catalyses 3′ end hydrolysis to generate a 3′OH. This is then used as a nucleophile to attack the opposite strand shedding both donor flanks. The Tpase then catalyses hydrolysis of the hairpin to produce free 3′OH ends, which then continue on to attack the target DNA.
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Further Reading

Craig N, Chandler M, Gellert M, Lambowitz A and Sandemeyer S (eds) (2015) Mobile DNA, vol. III. Washington DC: ASM Press.

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Chandler, Michael(Sep 2016) Transposons: Prokaryotic. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000591.pub2]