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Plasmid Partition Mechanisms

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  • Authors: Jamie C. Baxter1, Barbara E. Funnell2
  • Editors: Marcelo Tolmasky3, Juan Carlos Alonso4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada; 2: Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada; 3: California State University, Fullerton, CA; 4: Centro Nacional de Biotecnología, Cantoblanco, Madrid, Spain
  • Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
  • Received 07 May 2014 Accepted 08 May 2014 Published 07 November 2014
  • Barbara Funnell, b.funnell@utoronto.ca
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  • Abstract:

    The stable maintenance of low-copy-number plasmids in bacteria is actively driven by partition mechanisms that are responsible for the positioning of plasmids inside the cell. Partition systems are ubiquitous in the microbial world and are encoded by many bacterial chromosomes as well as plasmids. These systems, although different in sequence and mechanism, typically consist of two proteins and a DNA partition site, or prokaryotic centromere, on the plasmid or chromosome. One protein binds site-specifically to the centromere to form a partition complex, and the other protein uses the energy of nucleotide binding and hydrolysis to transport the plasmid, via interactions with this partition complex inside the cell. For plasmids, this minimal cassette is sufficient to direct proper segregation in bacterial cells. There has been significant progress in the last several years in our understanding of partition mechanisms. Two general areas that have developed are (i) the structural biology of partition proteins and their interactions with DNA and (ii) the action and dynamics of the partition ATPases that drive the process. In addition, systems that use tubulin-like GTPases to partition plasmids have recently been identified. In this chapter, we concentrate on these recent developments and the molecular details of plasmid partition mechanisms.

  • Citation: Baxter J, Funnell B. 2014. Plasmid Partition Mechanisms. Microbiol Spectrum 2(6):PLAS-0023-2014. doi:10.1128/microbiolspec.PLAS-0023-2014.

Key Concept Ranking

Bacterial Proteins
0.98135066
DNA
0.55455786
IHF Protein
0.50526315
0.98135066

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/content/journal/microbiolspec/10.1128/microbiolspec.PLAS-0023-2014
2014-11-07
2017-07-23

Abstract:

The stable maintenance of low-copy-number plasmids in bacteria is actively driven by partition mechanisms that are responsible for the positioning of plasmids inside the cell. Partition systems are ubiquitous in the microbial world and are encoded by many bacterial chromosomes as well as plasmids. These systems, although different in sequence and mechanism, typically consist of two proteins and a DNA partition site, or prokaryotic centromere, on the plasmid or chromosome. One protein binds site-specifically to the centromere to form a partition complex, and the other protein uses the energy of nucleotide binding and hydrolysis to transport the plasmid, via interactions with this partition complex inside the cell. For plasmids, this minimal cassette is sufficient to direct proper segregation in bacterial cells. There has been significant progress in the last several years in our understanding of partition mechanisms. Two general areas that have developed are (i) the structural biology of partition proteins and their interactions with DNA and (ii) the action and dynamics of the partition ATPases that drive the process. In addition, systems that use tubulin-like GTPases to partition plasmids have recently been identified. In this chapter, we concentrate on these recent developments and the molecular details of plasmid partition mechanisms.

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FIGURE 1

Structures of DNA binding domains of plasmid CBPs. (A–C) The DNA binding domains of HTH CBPs: (A) P1 ParB, (B) F SopB, and (C) RP4 KorB are shown bound to their respective centromere sequences (gray). The HTH motifs are in yellow. Residues that make base-specific contacts with the centromere DNA are shown as sticks (red) and can be found both within the HTH (ParB and SopB) and in the adjacent four-helix bundle (KorB). The dimerization domain of ParB is its second DNA binding domain (to the B-box DNA motif, green DNA). The ParB structure bridges across four DNA molecules ( 31 ). Because the dimer domains are absent in the structures of SopB and KorB, two monomers are presented interacting with the one inverted repeat sequence. Additional monomer-monomer contacts (cyan) in the SopB structure suggest it may also bridge across DNA molecules (not shown) ( 33 ). (D–H) The DNA binding regions of RHH CBPs. Type Ib CBPs of (D) TP228 ParG, (E) pCXC100 ParB, and (F) pSM19035 ω and type II ParRs of (G) pB171 and (H) pSK41 illustrate the simple β-strand dimerization and DNA binding [represented as red sticks in (F) and (H)] interface stabilized by α-helical interactions. Type-Ib CBPs contain a flexible N-terminal tail (not shown) that interacts with their cognate ATPase. Type II CBPs mediate their cognate ATPase contacts through the C-termini, present in the pB171 ParR structure (G). The C-terminal region of ParRs also promotes higher order assembly on DNA, yielding a super-helical structure, as illustrated by the crystal packing of the pSK41 ParR structure in (I). The electrostatic representation of the superhelical filament shows the electropositive surface (blue) interacting with the DNA and the electronegative surface (red) on the inside of the helical filament. The latter interface interacts with the predominantly electropositive surface of its cognate ATPase ParM and serves as a cap for stabilizing ParM filamentsin the cell. All structural images were generated using PyMOL v1.6.0.0 software (Schrödinger, LLC 2010). PDB information is listed in Table 2 . doi:10.1128/microbiolspec.PLAS-0023-2014.f1

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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FIGURE 2

Filamentation mechanisms of plasmid partition. The paradigm for type II partition is the ParMRC system of plasmid R1, illustrated here for (A) properties of filament growth and catastrophe and (B) plasmid partition in the bacterial cell. A critical concentration of ParM nucleates polymerization into filaments. ParM within the filaments hydrolyzes ATP to ADP, but as long as the filaments are capped with ParM-ATP or with ParR/ complexes, the filament is stable. Loss of the cap results in rapid depolymerization, or catastrophe. For ParM, each filament is a double-helical bundle of ParM. Antiparallel arrangement of these bundles results in bidirectional plasmid movement during partition. (C) Treadmilling by TubZ in type III partition systems. TubZ forms dynamic filaments, which grow at the plus (+) end by addition of TubZ-GTP and shrink at the minus (-) end by dissociation of TubZ-GDP. TubR associates with the C-terminal tail of TubZ. TubR/plasmid complexes move toward the plus direction as they are handed from one TubZ to the next in the polymer. Ni et al. have proposed that plasmids dissociate from the TubZ filament when it bends after contact with the curved cell pole ( 125 ). doi:10.1128/microbiolspec.PLAS-0023-2014.f2

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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FIGURE 3

ParM structures. The ParM structures from (A) R1 and (B) pSK41 are shown in the absence of nucleotide, the open state of these proteins. ATP binds in the central cleft, and the loops important for binding ATP are highlighted in green. The rest of the structure is colored according to the structural conservation (blue, most conserved; red, least conserved; gray, little to no identifiable conservation) through alignment with the actin structure (PDB 1yag, not shown). Most of the conservation with actin is in domains IA, IIA, and IIB. Domain IB of R1 ParM closes over the ATP binding pocket when nucleotide is present [direction of motion illustrated in (A)]. This cap serves to close the structure, forming the pointed end (domains IB and IIB) of the protein. During filament growth, the pointed end interacts with the barbed end (domains IA and IIA), as shown with the closed forms of ParM in (C). Binding of a ParR peptide induces a closer interaction between the pointed domains, which is proposed to either stabilize the filament to slow down ATP hydrolysis or prevent filament disassembly even in the presence of ATP hydrolysis. ParR binding is confined to the end of the filament because the interaction between the pointed and barbed interfaces of each monomer occludes the ParR binding site ( 74 ). All structural images were generated using PyMOL v1.6.0.0 software (Schrödinger, LLC 2010). PDB information is listed in Table 2 . doi:10.1128/microbiolspec.PLAS-0023-2014.f3

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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FIGURE 4

Structures of ParAs. (A–C) Structures of the nucleotide-bound forms of (A) P1 ParA (ADP), (B) pSM19035 δ (ATPγS), and (C) TP228 ParF (AMPPCP). Nucleotides are shown in red and magnesium, when present, in green. The structures are presented with their dimerization interfaces perpendicular to the viewing plane. (D–F) Surface charge electrostatics for monomer views of the above proteins are presented as electropositive (blue) or electronegative (red) and were generated with the Adaptive Poisson-Boltzmann Solver software ( 99 ). Structures were superimposed with the PyMOL software package, with similar orientations of each monomer [(D) ParA, (E) δ, and (F) ParF)] to expose the nucleotide binding pocket and dimerization surface. DNA binding regions are characteristically electropositive, such as the winged HTH in ParA (D). (G–I) Alignments of the nucleotide binding pockets of ParA, δ, and ParF. The structure of the protein backbone is shown, with the side-chains of critical residues represented as sticks. Nucleotides are in red and magnesium ions are in green. The phosphate-binding regions consist of three conserved motifs: (G) Walker A and A′, in purple and Walker B in orange in (H). Also shown in (G) is the signature lysine (blue) of ParA-like Walker A motifs. (I) The region highlighted in tan is structurally conserved among ParA proteins and provides multiple specific contacts with the adenine moiety. (J) The sequences of the nucleotide binding regions above are aligned with each other and with the overall secondary structure for ParA, δ, and ParF (α-helices in red, β-strands in blue). The Walker A, A′, and B motifs are indicated above the sequence alignment. All structural images were generated using PyMOL v1.6.0.0 software (Schrödinger, LLC 2010). PDB information is listed in Table 2 . doi:10.1128/microbiolspec.PLAS-0023-2014.f4

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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FIGURE 5

Diffusion-ratchet mechanism of plasmid partition. (A) ParA exists in two forms, one active to bind the nucleoid (ParA*, gray ovals) and one not, which is diffusible in the cytoplasm (ParA, white squares). The conversion between these two forms is slow and depends on the ATP binding cycle of ParA. In P1 ParA, the slow step is a specific conformational change after it binds ATP (ParA-ATP to ParA-ATP* [ 87 ], not shown). (B) ParB/plasmid complexes interact with ParA on the nucleoid, and this interaction stimulates the conversion of active ParA back to the diffusible form. Because the conversion to the active form is slow, the inactive form diffuses away from its original location, leaving a void of ParA on the nucleoid. (C–D) This movement continues as ParA rebinds ATP and is then converted back to the DNA binding active form. (E–F) When two plasmid complexes are present, they move toward the nearest, high concentration of ParA on the nucleoid, away from each other. doi:10.1128/microbiolspec.PLAS-0023-2014.f5

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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Tables

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TABLE 1

Plasmid partition system nomenclature

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014
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TABLE 2

Structures of plasmid partition proteins

Source: microbiolspec November 2014 vol. 2 no. 6 doi:10.1128/microbiolspec.PLAS-0023-2014

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