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Chapter 13 : Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE

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Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, Page 1 of 2

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Abstract:

In the early 1980s, conjugative transposons were defined as large DNA segments of bacterial chromosomes capable of “intercellular transposition,” i.e., fragments able to move from the chromosome of a donor bacterium to the chromosome of a recipient bacterium during cell-to-cell contact. All these mobile genetic elements were found in pathogenic low GC Gram-positive bacteria, conferred antibiotic resistance properties, and were often capable of integrating into a large array of different sites (for review, see references ). Characterization of the molecular mechanism allowing integration into and excision from the chromosome revealed that conjugative transposons such as Tn do not encode a DDE transposase, but rather a site-specific tyrosine recombinase. Fundamental differences in the molecular mechanism of DNA strand exchanges catalyzed by transposases and site-specific tyrosine recombinases, and subsequent identification of conjugative mobile elements integrating into a unique site of the bacterial chromosome in both Gram-positive and Gram-negative bacteria exposed the inadequacy of the naming “conjugative transposons.” In fact, at the time the confusion in the scientific community was such that, in some instances, related elements were mislabeled as conjugative plasmids, R factors, or integrating conjugative plasmids ( ). Two nomenclatures proposed to replace the obsolete term by a more adequate nomenclature: constin, an acronym that stands for conjugative, self-transmissible, integrating element, and ICE, an acronym for integrative and conjugative element ( ). Over the years the term ICE gained a broader acceptance among many authors to describe elements found in both Gram-positive and Gram-negative bacteria, so this term is used hereafter instead of conjugative transposon.

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014

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Figures

Image of Figure 1
Figure 1

General models of ssDNA and dsDNA conjugative transfer of ICEs. (A) In the donor cell, the ICE excises from the chromosome by site-specific recombination between the and attachment sites. Following excision, the relaxase (Mob) recognizes the origin of transfer () and cleaves the strand, thereby becoming covalently bound to the 5′ end of the nicked strand. The single-stranded nucleoprotein complex is displaced by RC replication and interacts with the type IV coupling protein (T4CP), which energizes the translocation of the relaxase-bound ssDNA through the T4SS. Once in the recipient cell, the relaxase ligates the ssDNA molecule and the complementary strand is synthesized prior to integration into the chromosome by site-specific recombination between the and sites. The same process is also generally thought to occur in the donor cell. (B) Like ICEs, AICEs excise from the chromosome by site-specific recombination. Prior to transfer the excised circular AICE undergoes RC replication. The FtsK-like transfer protein Tra recognizes the AICE and mediates the translocation of the double-stranded AICE DNA by forming a hexameric pore structure and by hydrolyzing ATP. As for ICEs, the AICE integrates into the chromosome by site-specific recombination. Alternatively, RC replication can occur in the recipient prior to integration into the chromosome. doi:10.1128/microbiolspec.MDNA3-0008-2014.f1

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Image of Figure 2
Figure 2

Schematic representation of the modular organization of ICEs and of the typical functional protein signatures associated with each module depending on the mode of DNA transfer (ssDNA vs dsDNA). Possible combinations of integration/excision, replication, and conjugative transfer modules are represented. Int, tyrosine recombinase; Int, serine recombinase; T4CP, type IV coupling protein (VirD4-like protein); T4SS, type IV secretion system; Tra, FtsK-like DNA translocation protein; RepSA, RepAM, and RepPP, replication initiator proteins; Prim-pol, bifunctional DNA primase/polymerase. The regulation module is extremely variable between families of ICEs. doi:10.1128/microbiolspec.MDNA3-0008-2014.f2

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Image of Figure 3
Figure 3

Comparison of the linear genetic maps of the conserved genes of SXT/R391 ICEs and IncA/C conjugative plasmids. Alignment of the conserved genes of the ICE SXT and IncA/C conjugative plasmid pIP1202. ORFs are color coded as follows: black, DNA processing and mating pair formation; dark gray, genes involved in regulation; light gray, genes involved in replication, recombination, or repair; white, genes of unknown function. Numbers shown in the middle represent % identity between the orthologous proteins encoded by SXT and pIP1202 (Genbank AY055428.1 and NC_009141, respectively). The positions of insertions of variable DNA in SXT/R391 ICEs and IncA/C plasmids are marked by arrowheads. The positions of the origins of transfer (), origin of replication (), and site-specific attachment site () are indicated. doi:10.1128/microbiolspec.MDNA3-0008-2014.f3

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Figure 4

Model of ICE-mediated activation and mobilization of an MGI. DNA-damaging agents trigger the SOS response, alleviating the SetR-mediated repression of . The transcriptional activator SetCD activates the expression of and genes of the ICE. SetCD also directly activates the expression of of the ICE and and , while Int catalyzes the excision of the ICE, and Int and RdfM mediate the excision of the MGI. Expression of the operons leads to the formation of the mating pore that will connect the donor and recipient cells, and deliver the DNA. Specific genes produce the mobilization proteins (TraI and MobI) that will recognize, bind to, and cleave the s on both the ICE and MGI. The nicked DNA bound to TraI is directed to the mating pore and translocated to the recipient cell. doi:10.1128/microbiolspec.MDNA3-0008-2014.f4

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Image of Figure 5
Figure 5

Genetic organization of the integrated ICE. ORFs are symbolized by arrowed boxes with their name above and color coded as follow: black, DNA processing and mating pair formation; dark gray, regulation; dashed light gray, recombination; dashed black and white, quorum sensing; white, genes of unknown function or that do not belong to ICE. The promoters are indicated by angled arrows. The position of the origin of transfer () and the site-specific attachment sites ( and ) are indicated and represented by a black star and gray rectangles, respectively. Transporters are represented by cylinders. Name of proteins are written with a capital and the host’s factors are underlined. The quorum sensing system of ICE produces both the phosphate RapI and the prepeptide PhrI (pre-PhrI). Pre-PhrI is exported and maturated by an unknown transporter. When the mature pentapeptide PhrI reaches a threshold concentration in the extracellular environment, it is imported by the oligopeptide permease Opp. In the cell, PhrI inhibits the phosphatase RapI. Regulation of ICE. ICE activation pathway is encompassed in a gray round-angled box. Both the phosphatase. The RapI and the activation of RecA in RecA* during the SOS response activate the protease ImmA. ImmA site-specifically cleaves the transcriptional regulator ImmR, allowing the transcription from , thereby activating ICE excision and transfer. The pathway leading to ICE quiescence as an integrated element is depicted in a white round-angled box. In the absence of ImmA activation, i.e., without induction of the SOS response or after RapI inactivation by the pentapeptide PhrI, ImmR represses and activates , leading to ICE quiescence. Besides RecA, the dynamics of ICE involves host factors, such as the transcriptional regulators AbrB and Rok, or the protease ClpP, that directly or indirectly inhibit ICE mobility. Intracellular replication of ICE initiated at requires the ICE-encoded relaxase NicK and the helicase processivity factor HelP, as well as the host-encoded helicase PcrA, DNA polymerase subunit PolC, processivity clamp DnaN, and single-strand DNA binding protein Ssb. doi:10.1128/microbiolspec.MDNA3-0008-2014.f5

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Image of Figure 6
Figure 6

Genetic organization of integrated ICE and ICE. The organization of the ICEs is indicated by lines delimiting the variable and the core regions, which encompass the regulation, conjugation, and recombination modules. ORFs are symbolized by arrowed boxes with their name above and color coded as follow: black, DNA processing and mating pair formation; dark gray, regulation; dashed light gray, recombination; horizontal dashed gray and black, restriction-modification; white, genes of unknown function or that do not belong to the ICE. The promoters and rho-independent terminators are indicated by angled arrows and stem-loops. The positions of the putative origin of transfer () and the site-specific attachment sites ( and ) are indicated and represented by black stars and gray rectangles, respectively. The light gray areas indicate related sequences with the percentage of nucleotide identity. doi:10.1128/microbiolspec.MDNA3-0008-2014.f6

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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Image of Figure 7
Figure 7

Model for accretion–mobilization of related ICEs and CIMEs. The ICE and the CIME are schematized in black and gray, respectively. The attachment sites () are symbolized by dashed rectangles with the direct repeats in black. The integration site is located at the 3′ end of a hypothetical gene represented by a white arrowed box. For accretion, an incoming ICE resulting from acquisition by conjugation integrates by site-specific recombination between its site and the closely related (or ) site of a nonautonomous CIME. The resulting CIME–ICE composite structure carries the of the CIME ( ), the of the ICE ( ), and an internal site. The subsequent recombination between and leads to the -mobilization of the CIME by the ICE, whereas the recombination between and leads to the excision of the ICE, each element being able to conjugate toward a recipient cell. doi:10.1128/microbiolspec.MDNA3-0008-2014.f7

Citation: Carraro N, Burrus V. 2015. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE, p 289-309. 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.MDNA3-0008-2014
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