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The Interplay between Different Stability Systems Contributes to Faithful Segregation: pSM19035 as a Model

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  • Authors: Andrea Volante1, Nora E. Soberón2, Silvia Ayora3, Juan C. Alonso4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CNB-CSIC, 28049 Madrid, Spain; 2: Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CNB-CSIC, 28049 Madrid, Spain; 3: Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CNB-CSIC, 28049 Madrid, Spain; 4: Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CNB-CSIC, 28049 Madrid, Spain; 5: California State University, Fullerton, CA; 6: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec August 2014 vol. 2 no. 4 doi:10.1128/microbiolspec.PLAS-0007-2013
  • Received 18 October 2013 Accepted 05 November 2013 Published 15 August 2014
  • Juan C. Alonso, jcalonso@cnb.csic.es
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  • Abstract:

    The pSM19035 low-copy-number θ-replicating plasmid encodes five segregation () loci that contribute to plasmid maintenance. These loci map outside of the minimal replicon. The locus comprises β recombinase and two sites, and includes and also the γ topoisomerase and two sites. Recombinase β plays a role both in maximizing random segregation by resolving plasmid dimers () and in catalyzing inversion between two inversely oriented sites. , in concert with , facilitates replication fork pausing at sites and overcomes the accumulation of “toxic” replication intermediates. The locus encodes ω, ε, and ζ genes. The short-lived ε antitoxin and the long-lived ζ toxin form an inactive ζεζ complex. Free ζ toxin halts cell proliferation upon decay of the ε antitoxin and enhances survival. If ε expression is not recovered, by loss of the plasmid, the toxin raises lethality. The locus comprises δ and ω genes and six sites. Proteins δ and ω, by forming complexes with and chromosomal DNA, pair the plasmid copies at the nucleoid, leading to the formation of a dynamic δ gradient that separates the plasmids to ensure roughly equal distribution to daughter cells at cell division. The locus, which comprises ω (or ω plus ω2) and sites, coordinates expression of genes that control copy number, better-than-random segregation, faithful partition, and antibiotic resistance. The interplay of the loci and with the locus facilitates almost absolute plasmid stability.

  • Citation: Volante A, Soberón N, Ayora S, Alonso J. 2014. The Interplay between Different Stability Systems Contributes to Faithful Segregation: pSM19035 as a Model. Microbiol Spectrum 2(4):PLAS-0007-2013. doi:10.1128/microbiolspec.PLAS-0007-2013.

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/content/journal/microbiolspec/10.1128/microbiolspec.PLAS-0007-2013
2014-08-15
2017-07-22

Abstract:

The pSM19035 low-copy-number θ-replicating plasmid encodes five segregation () loci that contribute to plasmid maintenance. These loci map outside of the minimal replicon. The locus comprises β recombinase and two sites, and includes and also the γ topoisomerase and two sites. Recombinase β plays a role both in maximizing random segregation by resolving plasmid dimers () and in catalyzing inversion between two inversely oriented sites. , in concert with , facilitates replication fork pausing at sites and overcomes the accumulation of “toxic” replication intermediates. The locus encodes ω, ε, and ζ genes. The short-lived ε antitoxin and the long-lived ζ toxin form an inactive ζεζ complex. Free ζ toxin halts cell proliferation upon decay of the ε antitoxin and enhances survival. If ε expression is not recovered, by loss of the plasmid, the toxin raises lethality. The locus comprises δ and ω genes and six sites. Proteins δ and ω, by forming complexes with and chromosomal DNA, pair the plasmid copies at the nucleoid, leading to the formation of a dynamic δ gradient that separates the plasmids to ensure roughly equal distribution to daughter cells at cell division. The locus, which comprises ω (or ω plus ω2) and sites, coordinates expression of genes that control copy number, better-than-random segregation, faithful partition, and antibiotic resistance. The interplay of the loci and with the locus facilitates almost absolute plasmid stability.

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FIGURE 1

Genome organization of plasmid pSM19035 and its derivatives. (A) pSM19035 or pDB101 duplicated sequences, which comprise ∼80 and 68% of the molecule, respectively, are indicated by thick arrows, and the unique NR1 and NR2 regions are indicated by thin lines. The region deleted in pDB101 is contained between residues 16737 and 26509 of pSM19035. pBT233 and pBT234 contain residues 1 to 9084 and 7972 to 17820 of pSM19035, respectively (represented by dashed lines in the map). Number 1 was chosen arbitrarily to be the first nucleotide of the ninth codon of copS. The loci involved in replication (rep) and segregation (seg) are indicated. The upstream region of the promoters of the copS, δ and ω genes, which constitute the six cis-acting centromere-like parS sites (red boxes), are blown up. A parS site consists of a variable number of contiguous 7-bp heptad repeats (iterons) symbolized by ▸ (in direct) or ◂ (invert orientation), and the number of repeats and their relative orientations are indicated. The colored outer thin arrows indicate the organization of the genes. For the sake of simplicity, the rep and seg loci are indicated only once although they are repeated twice. (B) The promoters (P), the mRNAs, and the genes are shown and denoted as boxes, wavy lanes, and rectangles, respectively. The leading-strand replication origin (oriS, orange), the lagging-strand replication origin (ssiA, light blue), the six sites (yellow), and the direction of replication (black arrows) are denoted. Protein ω2-mediated transcriptional repression is indicated (red ovals). The plasmid region involved in replication is marked as rep (involving CopS, RepS, and oriS and ssiA). The regions involved in stable segregation are five: segA2 and six site), segB12 and ζ), segB22, ω2, and six parS sites), segC (α, β2, γ, and ssiA and six sites) and segD2 and P cop, P δ, and P ω sites [denoted as red boxes]). doi:10.1128/microbiolspec.PLAS-0007-2013.f1.

Source: microbiolspec August 2014 vol. 2 no. 4 doi:10.1128/microbiolspec.PLAS-0007-2013
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FIGURE 2

Genetic organization in plasmids of the inc18 family. The genomic organization at the rep and seg loci of the relevant pSM19035, pIP816, pAMβ1, pIP501, pRE25, and pVEF3 (as representative of the pVEF series) plasmids is shown schematically. The conserved color code indicates that the gene products are highly conserved (>89% identity) within the family. The quotation marks surrounding a gene denote that this gene contains deletions and/or point mutations. Similar parS sites are linked by vertical broken lines. A double bar indicates that the corresponding gene/region is out of scale. In pRE25, the putative centromere sites of the second par system (segE) are indicated as red circles. doi:10.1128/microbiolspec.PLAS-0007-2013.f2.

Source: microbiolspec August 2014 vol. 2 no. 4 doi:10.1128/microbiolspec.PLAS-0007-2013
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FIGURE 3

Protein structures. (A) Structure of the ζε2ζ inactive heterotetramer. The atomic coordinates of the inactive ζε2ζ heterotetramer (74) were obtained from the 1GVN Protein Data Bank (PDB) entry. (B) Structure of the (δ·ATPγS·Mg2+)2 complex. The atomic coordinates of δ2 were derived from the 2OZE PDB entry (65). (C) Model of the three-dimensional structure of δ2 complexed with DNA. (D) The three-dimensional structure of the ω2Δ19 protein. The atomic coordinates of ω2Δ19 were derived from the 1IRQ PDB entry (88). (E) Three-dimensional structure model of ω2Δ19 bound to parS2 was derived from the 2BNW, 2BNZ, and 2CAX PDB entries (89). parS2 DNA is space filling, ω2Δ19 is orange/red ribbons, and the repeats are indicated below. The modeled structures were prepared with DeepView/Swiss-Pdb-Viewer 3.7. (F) Complexes formed by ω2 and δ2 upon binding to parS DNA. Protein ω2 bound to parS DNA led to the formation of a short-living partition complex 1 (PC1) (condition 1); and ω2 bound to parS DNA in the presence of δ2 (out of scale), in the apo form, led to the formation of a long-living partition complex 2 (PC2) (2); δ2 bound to PC1 led to segrosome complex (SC) formation (3); and the interaction of two SCs led to bridging complex (BC) formation (4). (G) Complexes formed by ω2 and δ2 upon binding to non-parS DNA. Protein δ2 bound to DNA leading to dynamic complex (DC) formation (1); ω2 binding to DC led to a transient complex (TC) (2); the interaction of one TC and one DC led to pseudo-bridging complex 2 (BC2) formation (3); and the interaction of one SC and one TC led to bridging complex 1 (BC1) formation (4). doi:10.1128/microbiolspec.PLAS-0007-2013.f3.

Source: microbiolspec August 2014 vol. 2 no. 4 doi:10.1128/microbiolspec.PLAS-0007-2013
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FIGURE 4

Conserved organization of the segD locus. (A) The P copS , P δ, and P ω regions of plasmid pSM19035a, P copR or P copF of pIP501b or pAMβ1c, P ω2 of pIP501b or pAMβ1c, P δ of pAMβ1c, pRE25d and pVEF3e are indicated. The variable number of contiguous 7-bp heptad repeats (iterons) and their relative orientations (→ or ←) are shown. The P ω region is highly conserved among plasmids of the inc18 family. (B) Sequence alignment of the transcriptional repressors ω2 and their highly relative ω22. The alignment was done by using Clustal W2 and visualized with default coloring of the different residues by using Jalview v 14.0. (C) Conserved genetic organization of the ermB locus. The open reading frames and their relative orientations are represented by arrows. The erm gene coding for the leader peptide and ermB are denoted in dark gray (arrowhead and arrow, respectively), and the conserved downstream gene in light gray. The genes of the segB1, segB2, and segC loci are indicated. The ω2 or ω22 proteins are denoted by red and pink arrowheads, respectively, and the Ps sensitive to ω2 or ω22 repression are denoted as red boxes. Traces of a given gene are denoted by broken-line squares with the name of the gene indicated (e.g., pSM19035 containing traces of ω22). Fusions (e.g., pLM300 where ω2 was fused to an upstream gene) or deletions (e.g., pIP501 contains a deletion in the ζ gene) are also indicated. Similar organization was observed in pAM77 and pLUL631. doi:10.1128/microbiolspec.PLAS-0007-2013.f4.

Source: microbiolspec August 2014 vol. 2 no. 4 doi:10.1128/microbiolspec.PLAS-0007-2013
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