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Chapter 6 : The Integron: Adaptation On Demand

Authors: José Antonio Escudero*1, Céline Loot*3, Aleksandra Nivina5, Didier Mazel8
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Affiliations: 1: Institut Pasteur, Unité Plasticité du Génome Bactérien, 75724 Paris, France; 2: CNRS UMR3525, 75724 Paris, France; 3: Institut Pasteur, Unité Plasticité du Génome Bactérien, 75724 Paris, France; 4: CNRS UMR3525, 75724 Paris, France; 5: Institut Pasteur, Unité Plasticité du Génome Bactérien, 75724 Paris, France; 6: CNRS UMR3525, 75724 Paris, France; 7: Paris Descartes, Sorbonne Paris Cité, Paris, France; 8: Institut Pasteur, Unité Plasticité du Génome Bactérien, 75724 Paris, France; 9: CNRS UMR3525, 75724 Paris, France
Content Type: Monograph
Publication Year: 2015

Category: Clinical Microbiology

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Abstract:

Integrons are genetic platforms that allow bacteria to evolve rapidly through the acquisition, stockpiling, excision, and reordering of open reading frames found in mobile elements named cassettes. The evolutionary potency that integrons provide for bacteria is based on the variety of functions encoded in the cassettes, as well as on the intricate coupling of integron activity to bacterial stress ( ).

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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The Integron: Adaptation On Demand
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Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
/content/10.1128/9781555819217.chap6.fig6-1
Figure 1
Organization of integrons. (A) Insertion and excision of cassettes: the functional platform, composed of the integrase-encoding gene, the cassette (P) and integrase promoters (Pint), and the primary recombination site (red triangle), is shown. Cassette insertion ( × ) and excision ( ×  catalyzed by the IntI integrase are represented. Hybrid and sites are indicated. Arrows inside the cassettes indicate the direction of the open reading frame. (B) Expression of cassettes: cassettes of the array are represented by small arrows. Their expression level is reflected by the color intensity of each arrow. Only the first cassettes of the array are expressed, and the subsequent ones can be seen as a low-cost cassette reservoir.
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Figure 1

Organization of integrons. (A) Insertion and excision of cassettes: the functional platform, composed of the integrase-encoding gene, the cassette (P) and integrase promoters (Pint), and the primary recombination site (red triangle), is shown. Cassette insertion ( × ) and excision ( ×  catalyzed by the IntI integrase are represented. Hybrid and sites are indicated. Arrows inside the cassettes indicate the direction of the open reading frame. (B) Expression of cassettes: cassettes of the array are represented by small arrows. Their expression level is reflected by the color intensity of each arrow. Only the first cassettes of the array are expressed, and the subsequent ones can be seen as a low-cost cassette reservoir.

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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Figure 2
Integron recombination sites. The putative IntI1 binding domains are marked with green boxes. The black arrows show the cleavage points. (A) Sequence of the double-stranded site: inverted repeats (R and L) and direct repeats (DR1 and DR2) are indicated with gray arrows. (B) Schematic representation of double-stranded (ds) sites; inverted repeats (R”, L” L’, and R’) are indicated with gray arrows. The dotted lines represent the variable central part. The conserved nucleotides are indicated. Asterisks (*) show the conserved G nucleotides, which generate extrahelical bases (EHB) in the folded site bottom strand (bs). The top strand (ts) and bottom strand (bs) are marked. (C) Proposed secondary structures of the and VCR bottom strands: structures were determined by the UNAFOLD online interface at the Institut Pasteur. Structural features of sites, namely, the Unpaired Central Spacer (UCS), the ExtraHelical Bases (EHBs), the stem and the Variable Terminal Structure (VTS) are indicated. Asterisks (*) show the conserved G extrahelical base. The conserved triplet (CT) is indicated. Primary sequences of the sites are shown (except for the VTS of the VCR site). (D) Schematic representation of structural features of the VCR site and their roles: the structural features and their roles are indicated.
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Figure 2

Integron recombination sites. The putative IntI1 binding domains are marked with green boxes. The black arrows show the cleavage points. (A) Sequence of the double-stranded site: inverted repeats (R and L) and direct repeats (DR1 and DR2) are indicated with gray arrows. (B) Schematic representation of double-stranded (ds) sites; inverted repeats (R”, L” L’, and R’) are indicated with gray arrows. The dotted lines represent the variable central part. The conserved nucleotides are indicated. Asterisks (*) show the conserved G nucleotides, which generate extrahelical bases (EHB) in the folded site bottom strand (bs). The top strand (ts) and bottom strand (bs) are marked. (C) Proposed secondary structures of the and VCR bottom strands: structures were determined by the UNAFOLD online interface at the Institut Pasteur. Structural features of sites, namely, the Unpaired Central Spacer (UCS), the ExtraHelical Bases (EHBs), the stem and the Variable Terminal Structure (VTS) are indicated. Asterisks (*) show the conserved G extrahelical base. The conserved triplet (CT) is indicated. Primary sequences of the sites are shown (except for the VTS of the VCR site). (D) Schematic representation of structural features of the VCR site and their roles: the structural features and their roles are indicated.

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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Figure 3
Replicative resolution of integron cassette insertion. Recombination between a double-stranded site (bold red lines) and a single-stranded bottom site (bold green lines) terminating a cassette is shown. The top strand of the site is represented as a dotted line because we do not exactly know the nature of the cassettes (ss or ds). The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). Classical resolution gives rise to covalently closed abortive molecules. The non-abortive resolution implies a replication step. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Both products are represented: the initial substrate resulting from the top strand replication, and the molecule containing the inserted cassette resulting from the bottom strand replication. Hybrid and sites are indicated.
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Figure 3

Replicative resolution of integron cassette insertion. Recombination between a double-stranded site (bold red lines) and a single-stranded bottom site (bold green lines) terminating a cassette is shown. The top strand of the site is represented as a dotted line because we do not exactly know the nature of the cassettes (ss or ds). The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). Classical resolution gives rise to covalently closed abortive molecules. The non-abortive resolution implies a replication step. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Both products are represented: the initial substrate resulting from the top strand replication, and the molecule containing the inserted cassette resulting from the bottom strand replication. Hybrid and sites are indicated.

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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Figure 4
Replicative resolution model of integron cassette excision. Recombination between two single-stranded bottom sites (bold green and pink lines) is shown. Top strands of sites are represented as dotted lines. The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). The proposed aHJ resolution model implying a replication step is based on the  ×  recombination. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: on one hand, the initial substrate resulting from the top strand replication, and on the other, the excised cassette (cassette) and the molecule devoid of the excised cassette (cassette 2 excised) both resulting from the bottom strand replication. Hybrid sites are indicated.
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Figure 4

Replicative resolution model of integron cassette excision. Recombination between two single-stranded bottom sites (bold green and pink lines) is shown. Top strands of sites are represented as dotted lines. The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). The proposed aHJ resolution model implying a replication step is based on the  ×  recombination. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: on one hand, the initial substrate resulting from the top strand replication, and on the other, the excised cassette (cassette) and the molecule devoid of the excised cassette (cassette 2 excised) both resulting from the bottom strand replication. Hybrid sites are indicated.

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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Figure 5
Two resolution pathways proposed for  ×  recombination. Recombination between two double-stranded sites (bold green and pink lines) is shown. The first proposed pathway is similar to the classical site-specific recombination catalyzed by Y-recombinases. The synaptic complex comprises two DNA duplexes bound by four recombinase protomers. The first two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form a HJ. Isomerization of this junction alternates the catalytic activity between the two pairs of protomers (dark and light-gray ovals) ensuring the second strand exchange and recombination product formation (co-integrate). The second pathway proposes a resolution of the HJ by replication. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: two initial substrates resulting from the top strand replication and co-integrate resulting from the bottom strand replication. Hybrid sites are indicated.
10.1128/9781555819217/fig6-5_thmb.gif
10.1128/9781555819217/fig6-5.gif
Image of Figure 5
Figure 5

Two resolution pathways proposed for  ×  recombination. Recombination between two double-stranded sites (bold green and pink lines) is shown. The first proposed pathway is similar to the classical site-specific recombination catalyzed by Y-recombinases. The synaptic complex comprises two DNA duplexes bound by four recombinase protomers. The first two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form a HJ. Isomerization of this junction alternates the catalytic activity between the two pairs of protomers (dark and light-gray ovals) ensuring the second strand exchange and recombination product formation (co-integrate). The second pathway proposes a resolution of the HJ by replication. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: two initial substrates resulting from the top strand replication and co-integrate resulting from the bottom strand replication. Hybrid sites are indicated.

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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Figure 6
Intimate connection between the integron and cell physiology. A snapshot representation of the links between integrons’ activity and bacterial physiology is shown. The main triggering signal for integrase expression is the bacterial SOS response. A detailed description of these connections is depicted in the section entitled:
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Figure 6

Intimate connection between the integron and cell physiology. A snapshot representation of the links between integrons’ activity and bacterial physiology is shown. The main triggering signal for integrase expression is the bacterial SOS response. A detailed description of these connections is depicted in the section entitled:

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. 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.MDNA3-0019-2014
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