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

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  • Authors: Nicolas Carraro1, Vincent Burrus2
  • Editors: Phoebe Rice3, Nancy Craig4
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    Affiliations: 1: Département de Biologie, Faculté des Sciences, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1 Canada; 2: Département de Biologie, Faculté des Sciences, Université de Sherbrooke, Sherbrooke, QC, J1K 2R1 Canada; 3: University of Chicago, Chicago, IL; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
  • Received 03 June 2014 Accepted 23 June 2014 Published 19 December 2014
  • Vincent Burrus, vincent.burrus@usherbrooke.ca
image of Biology of Three ICE Families: SXT/R391, ICE<span class="jp-italic">Bs1</span>, and ICE<span class="jp-italic">St1</span>/ICE<span class="jp-italic">St3</span>
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  • Abstract:

    Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

  • Citation: Carraro N, Burrus V. 2014. Biology of Three ICE Families: SXT/R391, ICE, and ICE/ICE. Microbiol Spectrum 2(6):MDNA3-0008-2014. doi:10.1128/microbiolspec.MDNA3-0008-2014.

Key Concept Ranking

Mobile Genetic Elements
0.6386785
Bacterial Mobile Genetic Elements
0.47175175
Genetic Elements
0.405827
Type IV Secretion Systems
0.4047462
0.6386785

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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0008-2014
2014-12-19
2017-11-23

Abstract:

Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

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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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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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

Source: microbiolspec December 2014 vol. 2 no. 6 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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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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

Source: microbiolspec December 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.MDNA3-0008-2014
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