General Information/Target Choice

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The influence of different IS on genome architecture will depend not only on their levels of activity but also on the type of target into which they insert. It was initially believed that TE show no or only low sequence specificity in their target choice. For example IS630 and the eukaryotic Tc/mariner families[1] both require a TA dinucleotide in the target [2][3] while others such as the IS200/IS605 and IS91 families require short tetra- or penta-nucleotide sequences[4][5]. Yet others, such as IS1 and IS186 (of the IS4 family), show some regional specificity (for AT and GC rich sequences respectively) [6][7][8].

Although, from a global genome perspective, insertion may appear to occur without significant sequence specificity, accumulation of more statistically robust data has uncovered rather subtler insertion patterns revealing that several TE use rather shrewd mechanisms in choosing a target. For example, there is some indication from the public databases suggesting that IS density is generally significantly higher in conjugative bacterial plasmids than in their host chromosomes, with the exception of special cases in which the host has undergone IS expansion. Such plasmids are major vectors in lateral gene transfer and are important vectors in IS transmission (as well as in transmission of accessory traits such as resistance to antibacterials). Some TE, including IS, appear to be attracted to replication forks[9][10][11] and show a strong orientation bias indicating strand preference at the fork[9][12][11][13][14]. Moreover, in certain cases, insertion may target stalled replication forks[15]. A link between replication (in this case, replication origins) and insertion has also now been observed for a eukaryotic TE: the P element of Drosophila[16].

For example, transposon Tn7 has two modes of transposition[17][18][19] (see "Tn7 family"): in one, which uses the Tn7-encoded target protein TnsD, a specific sequence within the highly conserved glmS is recognized and insertion occurs next to this essential gene[11][17][20][21]; in the second, which uses a more general targeting protein, TnsE, insertion occurs into replication forks directed by interactions with the β-clamp[22][23]. This latter pathway results in a strong orientation bias of Tn7 insertions, consistent with insertion into the lagging strand of the replication fork formed during conjugative transfer. Although studies with IS are less advanced, a similar orientation bias was observed with IS903[13][14], suggesting that it too may use the β-clamp in directing insertions. It seems probable that many other IS use this type of protein-protein interaction.

The second example of a specialized target choice was observed in members of the IS200/IS605 family (see "IS200/IS605-family"). These transpose using a strand-specific single-strand intermediate and insertion occurs 3’ to a tetra- or pentanucleotide on the lagging strand[24][15]. Clear vestiges of this specificity can still be detected in a large number of bacterial genomes, where the orientation of insertion is strongly correlated with the direction of replication. There are clearly incidences of insertion in the “wrong” orientation, but many of these may be explained by post-insertion genome rearrangements involving inversions. This would place the “active” strand of the IS on the lagging rather than on the leading strand. Interestingly, those IS which are not oriented in the “correct” orientation with respect to replication are almost certainly inactive and unable to transpose further[24].

Other examples of sequence-specific target choice have been described. IS1, for example, shows a preference for regions rich in AT whereas the transposon TnGBS (an ICE from Steptococcus agalactiae) and members of the closely related ISLre2 family show a preference for insertion 15-17bp upstream of σA promoters[25][26]. Targeting of upstream regions of transcription units has also been extensively documented for certain eukaryotic transposons (e.g. [27][28]).

Potential topological characteristics or secondary structures are another feature which can attract certain TE. Changes in topology induced by the nucleoid protein, H-NS, for example, may explain the effects of H-NS mutants on the target choice of IS903 and Tn10 (IS10)[29][30]. Members of the IS110, IS3 and IS4 families are examples of IS which insert into potential secondary structures such as Repeated Extragenic Palindromes (REP)[15][31][32][33], integrons[34][35] or even the ends of other TE[36][37] .

Some transposons such as Tn7 in Escherichia coli[38] and Tn917 in Bacillus subtilis[39], Enterococcus faecalis[40] and Streptococcus equi (but not in Listeria monocytogenes or Streptococcus suis)[41] also show a preference for integration into the replication terminus region and sites of DNA breakage may also attract insertions[38]. Interestingly, an analysis of incorporation of “self-DNA” by a CRISPR system in E. coli showed a preference for trapping DNA from the terminus region of the chromosome[42], mimicking the target preference of Tn7. It remains to be seen whether any IS has adopted these types of target preference.

In addition, IS21, IS30 and IS911 have all been observed to insert close to sequences which resemble their own IR[43][44][45][46]. Although these IS are members of different families, they have in common the formation of a dsDNA excised circular transposon intermediate with abutted left and right ends[47]. Insertion next to a resident “target” IR such that IR of the IS are abutted “head-to-head” presumably reflects the capacity of the Tpase to form a synaptic complex between one IR present in the transposon circle and the target IR. This type of structure is extremely active in transposition and will continue to generate genome rearrangements.

It has also been observed that certain transposons, in particular members of the Tn7 family, carry CRISPR-Cas proteins[48][49][50]. The function of CRISPR-cas systems is generally to provide adaptive immunity against invading bacterial and archaeal viruses and other mobile genetic elements. When incorporated as part of a Tn7 family member, the CRISPR/Cas systems have been subverted and do not retain their defense functions against incoming mobile genetic elements. Instead, they have been “repurposed“[51] to use guide RNAs to target Tn insertion.

These examples represent only a small part of the literature concerning factors influencing target choice, but serve to illustrate the impact this can have on genomes.

Bibliography

  1. ↑ Tellier M, Bouuaert CC, Chalmers R . Mariner and the ITm Superfamily of Transposons. - Microbiol Spectr: 2015 Apr, 3(2);MDNA3-0033-2014. [PubMed:26104691] [DOI]
  2. ↑ Feng X, Colloms SD . In vitro transposition of ISY100, a bacterial insertion sequence belonging to the Tc1/mariner family. - Mol Microbiol: 2007 Sep, 65(6);1432-43 [PubMed:17680987] [DOI]
  3. ↑ Plasterk RH . The Tc1/mariner transposon family. - Curr Top Microbiol Immunol: 1996, 204;125-43 [PubMed:8556864] [DOI]
  4. ↑ Mendiola MV, de la Cruz F . Specificity of insertion of IS91, an insertion sequence present in alpha-haemolysin plasmids of Escherichia coli. - Mol Microbiol: 1989 Jul, 3(7);979-84 [PubMed:2552258] [DOI]
  5. ↑ Guynet C, Achard A, Hoang BT, Barabas O, Hickman AB, Dyda F, Chandler M . Resetting the site: redirecting integration of an insertion sequence in a predictable way. - Mol Cell: 2009 Jun 12, 34(5);612-9 [PubMed:19524540] [DOI]
  6. ↑ Galas DJ, Calos MP, Miller JH . Sequence analysis of Tn9 insertions in the lacZ gene. - J Mol Biol: 1980 Nov 25, 144(1);19-41 [PubMed:6260963] [DOI]
  7. ↑ Meyer J, Iida S, Arber W . Does the insertion element IS1 transpose preferentially into A+T-rich DNA segments? - Mol Gen Genet: 1980, 178(2);471-3 [PubMed:6248730] [DOI]
  8. ↑ Sengstag C, Iida S, Hiestand-Nauer R, Arber W . Terminal inverted repeats of prokaryotic transposable element IS186 which can generate duplications of variable length at an identical target sequence. - Gene: 1986, 49(1);153-6 [PubMed:3032747] [DOI]
  9. ↑ 9.0 9.1 Peters JE, Craig NL . Tn7 recognizes transposition target structures associated with DNA replication using the DNA-binding protein TnsE. - Genes Dev: 2001 Mar 15, 15(6);737-47 [PubMed:11274058] [DOI]
  10. ↑ Ton-Hoang B, Pasternak C, Siguier P, Guynet C, Hickman AB, Dyda F, Sommer S, Chandler M . Single-stranded DNA transposition is coupled to host replication. - Cell: 2010 Aug 6, 142(3);398-408 [PubMed:20691900] [DOI]
  11. ↑ 11.0 11.1 11.2 Peters JE, Craig NL . Tn7: smarter than we thought. - Nat Rev Mol Cell Biol: 2001 Nov, 2(11);806-14 [PubMed:11715047] [DOI]
  12. ↑ Ton-Hoang B, Pasternak C, Siguier P, Guynet C, Hickman AB, Dyda F, Sommer S, Chandler M . Single-stranded DNA transposition is coupled to host replication. - Cell: 2010 Aug 6, 142(3);398-408 [PubMed:20691900] [DOI]
  13. ↑ 13.0 13.1 Hu WY, Derbyshire KM . Target choice and orientation preference of the insertion sequence IS903. - J Bacteriol: 1998 Jun, 180(12);3039-48 [PubMed:9620951] [DOI]
  14. ↑ 14.0 14.1 Hu WY, Thompson W, Lawrence CE, Derbyshire KM . Anatomy of a preferred target site for the bacterial insertion sequence IS903. - J Mol Biol: 2001 Feb 23, 306(3);403-16 [PubMed:11178901] [DOI]
  15. ↑ 15.0 15.1 15.2 He S, Corneloup A, Guynet C, Lavatine L, Caumont-Sarcos A, Siguier P, Marty B, Dyda F, Chandler M, Ton Hoang B . The IS200/IS605 Family and "Peel and Paste" Single-strand Transposition Mechanism. - Microbiol Spectr: 2015 Aug, 3(4); [PubMed:26350330] [DOI]
  16. ↑ Spradling AC, Bellen HJ, Hoskins RA . Drosophila P elements preferentially transpose to replication origins. - Proc Natl Acad Sci U S A: 2011 Sep 20, 108(38);15948-53 [PubMed:21896744] [DOI]
  17. ↑ 17.0 17.1 Peters JE . Tn7. - Microbiol Spectr: 2014 Oct, 2(5); [PubMed:26104363] [DOI]
  18. ↑ Craig NL . Tn7: a target site-specific transposon. - Mol Microbiol: 1991 Nov, 5(11);2569-73 [PubMed:1664019] [DOI]
  19. ↑ Waddell CS, Craig NL . Tn7 transposition: two transposition pathways directed by five Tn7-encoded genes. - Genes Dev: 1988 Feb, 2(2);137-49 [PubMed:2834269] [DOI]
  20. ↑ McKown RL, Orle KA, Chen T, Craig NL . Sequence requirements of Escherichia coli attTn7, a specific site of transposon Tn7 insertion. - J Bacteriol: 1988 Jan, 170(1);352-8 [PubMed:2826397] [DOI]
  21. ↑ Waddell CS, Craig NL . Tn7 transposition: recognition of the attTn7 target sequence. - Proc Natl Acad Sci U S A: 1989 Jun, 86(11);3958-62 [PubMed:2542960] [DOI]
  22. ↑ Parks AR, Li Z, Shi Q, Owens RM, Jin MM, Peters JE . Transposition into replicating DNA occurs through interaction with the processivity factor. - Cell: 2009 Aug 21, 138(4);685-95 [PubMed:19703395] [DOI]
  23. ↑ Wolkow CA, DeBoy RT, Craig NL . Conjugating plasmids are preferred targets for Tn7. - Genes Dev: 1996 Sep 1, 10(17);2145-57 [PubMed:8804309] [DOI]
  24. ↑ 24.0 24.1 Ton-Hoang B, Pasternak C, Siguier P, Guynet C, Hickman AB, Dyda F, Sommer S, Chandler M . Single-stranded DNA transposition is coupled to host replication. - Cell: 2010 Aug 6, 142(3);398-408 [PubMed:20691900] [DOI]
  25. ↑ Brochet M, Da Cunha V, Couvé E, Rusniok C, Trieu-Cuot P, Glaser P . Atypical association of DDE transposition with conjugation specifies a new family of mobile elements. - Mol Microbiol: 2009 Feb, 71(4);948-59 [PubMed:19183283] [DOI]
  26. ↑ Guérillot R, Da Cunha V, Sauvage E, Bouchier C, Glaser P . Modular evolution of TnGBSs, a new family of integrative and conjugative elements associating insertion sequence transposition, plasmid replication, and conjugation for their spreading. - J Bacteriol: 2013 May, 195(9);1979-90 [PubMed:23435978] [DOI]
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  29. ↑ Swingle B, O'Carroll M, Haniford D, Derbyshire KM . The effect of host-encoded nucleoid proteins on transposition: H-NS influences targeting of both IS903 and Tn10. - Mol Microbiol: 2004 May, 52(4);1055-67 [PubMed:15130124] [DOI]
  30. ↑ Haniford DB, Ellis MJ . Transposons Tn10 and Tn5. - Microbiol Spectr: 2015 Feb, 3(1);MDNA3-0002-2014 [PubMed:26104553] [DOI]
  31. ↑ Wilde C, Escartin F, Kokeguchi S, Latour-Lambert P, Lectard A, Clément JM . Transposases are responsible for the target specificity of IS1397 and ISKpn1 for two different types of palindromic units (PUs). - Nucleic Acids Res: 2003 Aug 1, 31(15);4345-53 [PubMed:12888493] [DOI]
  32. ↑ Clément JM, Wilde C, Bachellier S, Lambert P, Hofnung M . IS1397 is active for transposition into the chromosome of Escherichia coli K-12 and inserts specifically into palindromic units of bacterial interspersed mosaic elements. - J Bacteriol: 1999 Nov, 181(22);6929-36 [PubMed:10559158] [DOI]
  33. ↑ Tobes R, Pareja E . Bacterial repetitive extragenic palindromic sequences are DNA targets for Insertion Sequence elements. - BMC Genomics: 2006 Mar 24, 7;62 [PubMed:16563168] [DOI]
  34. ↑ Tetu SG, Holmes AJ . A family of insertion sequences that impacts integrons by specific targeting of gene cassette recombination sites, the IS1111-attC Group. - J Bacteriol: 2008 Jul, 190(14);4959-70 [PubMed:18487340] [DOI]
  35. ↑ Post V, Hall RM . Insertion sequences in the IS1111 family that target the attC recombination sites of integron-associated gene cassettes. - FEMS Microbiol Lett: 2009 Jan, 290(2);182-7 [PubMed:19025573] [DOI]
  36. ↑ Hallet B, Rezsöhazy R, Delcour J . IS231A from Bacillus thuringiensis is functional in Escherichia coli: transposition and insertion specificity. - J Bacteriol: 1991 Jul, 173(14);4526-9 [PubMed:1648561] [DOI]
  37. ↑ Partridge SR, Hall RM . The IS1111 family members IS4321 and IS5075 have subterminal inverted repeats and target the terminal inverted repeats of Tn21 family transposons. - J Bacteriol: 2003 Nov, 185(21);6371-84 [PubMed:14563872] [DOI]
  38. ↑ 38.0 38.1 Peters JE, Craig NL . Tn7 transposes proximal to DNA double-strand breaks and into regions where chromosomal DNA replication terminates. - Mol Cell: 2000 Sep, 6(3);573-82 [PubMed:11030337] [DOI] &
  39. ↑ Shi Q, Huguet-Tapia JC, Peters JE . Tn917 targets the region where DNA replication terminates in Bacillus subtilis, highlighting a difference in chromosome processing in the firmicutes. - J Bacteriol: 2009 Dec, 191(24);7623-7 [PubMed:19820088] [DOI]
  40. ↑ Garsin DA, Urbach J, Huguet-Tapia JC, Peters JE, Ausubel FM . Construction of an Enterococcus faecalis Tn917-mediated-gene-disruption library offers insight into Tn917 insertion patterns. - J Bacteriol: 2004 Nov, 186(21);7280-9 [PubMed:15489440] [DOI]
  41. ↑ Slater JD, Allen AG, May JP, Bolitho S, Lindsay H, Maskell DJ . Mutagenesis of Streptococcus equi and Streptococcus suis by transposon Tn917. - Vet Microbiol: 2003 May 29, 93(3);197-206 [PubMed:12695044] [DOI]
  42. ↑ Levy A, Goren MG, Yosef I, Auster O, Manor M, Amitai G, Edgar R, Qimron U, Sorek R . CRISPR adaptation biases explain preference for acquisition of foreign DNA. - Nature: 2015 Apr 23, 520(7548);505-510 [PubMed:25874675] [DOI]
  43. ↑ Reimmann C, Haas D . Mode of replicon fusion mediated by the duplicated insertion sequence IS21 in Escherichia coli. - Genetics: 1987 Apr, 115(4);619-25 [PubMed:3034717] [DOI]
  44. ↑ Prère MF, Chandler M, Fayet O . Transposition in Shigella dysenteriae: isolation and analysis of IS911, a new member of the IS3 group of insertion sequences. - J Bacteriol: 1990 Jul, 172(7);4090-9 [PubMed:2163395] [DOI]
  45. ↑ Olasz F, Farkas T, Kiss J, Arini A, Arber W . Terminal inverted repeats of insertion sequence IS30 serve as targets for transposition. - J Bacteriol: 1997 Dec, 179(23);7551-8 [PubMed:9393723] [DOI]
  46. ↑ Loot C, Turlan C, Chandler M . Host processing of branched DNA intermediates is involved in targeted transposition of IS911. - Mol Microbiol: 2004 Jan, 51(2);385-93 [PubMed:14756780] [DOI]
  47. ↑ Chandler M, Fayet O, Rousseau P, Ton Hoang B, Duval-Valentin G . Copy-out-Paste-in Transposition of IS911: A Major Transposition Pathway. - Microbiol Spectr: 2015 Aug, 3(4); [PubMed:26350305] [DOI]
  48. ↑ Peters JE, Makarova KS, Shmakov S, Koonin EV . Recruitment of CRISPR-Cas systems by Tn7-like transposons. - Proc Natl Acad Sci U S A: 2017 Aug 29, 114(35);E7358-E7366 [PubMed:28811374] [DOI]
  49. ↑ McDonald ND, Regmi A, Morreale DP, Borowski JD, Boyd EF . CRISPR-Cas systems are present predominantly on mobile genetic elements in Vibrio species. - BMC Genomics: 2019 Feb 4, 20(1);105 [PubMed:30717668] [DOI]
  50. ↑ Faure G, Shmakov SA, Yan WX, Cheng DR, Scott DA, Peters JE, Makarova KS, Koonin EV . CRISPR-Cas in mobile genetic elements: counter-defence and beyond. - Nat Rev Microbiol: 2019 Aug, 17(8);513-525 [PubMed:31165781] [DOI]
  51. ↑ Peters JE . Targeted transposition with Tn7 elements: safe sites, mobile plasmids, CRISPR/Cas and beyond. - Mol Microbiol: 2019 Dec, 112(6);1635-1644 [PubMed:31502713] [DOI]


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