P1 Plasmid Segregation: Accurate Redistribution by Dynamic Plasmid Pairing and Separation

Sengupta, Manjistha; Nielsen, Hans Jørgen; Youngren, Brenda; Austin, Stuart

doi:10.1128/jb.01245-09

Cited by 77 publications

(101 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The copy number of the plasmid is estimated to approximately five per cell based on published information (21). The plasmid pBM22 contained the parFG-mCherry-parH module and a lacO 120 array (37).…”

Section: Methodsmentioning

confidence: 99%

A three-dimensional ParF meshwork assembles through the nucleoid to mediate plasmid segregation

et al. 2016

View full text Add to dashboard Cite

Genome segregation is a fundamental step in the life cycle of every cell. Most bacteria rely on dedicated DNA partition proteins to actively segregate chromosomes and low copy-number plasmids. Here, by employing super resolution microscopy, we establish that the ParF DNA partition protein of the ParA family assembles into a three-dimensional meshwork that uses the nucleoid as a scaffold and periodically shuttles between its poles. Whereas ParF specifies the territory for plasmid trafficking, the ParG partner protein dictates the tempo of ParF assembly cycles and plasmid segregation events by stimulating ParF adenosine triphosphate hydrolysis. Mutants in which this ParG temporal regulation is ablated show partition deficient phenotypes as a result of either altered ParF structure or dynamics and indicate that ParF nucleoid localization and dynamic relocation, although necessary, are not sufficient per se to ensure plasmid segregation. We propose a Venus flytrap model that merges the concepts of ParA polymerization and gradient formation and speculate that a transient, dynamic network of intersecting polymers that branches into the nucleoid interior is a widespread mechanism to distribute sizeable cargos within prokaryotic cells.

show abstract

Section: Methodsmentioning

confidence: 99%

A three-dimensional ParF meshwork assembles through the nucleoid to mediate plasmid segregation

et al. 2016

View full text Add to dashboard Cite

show abstract

“…In vivo studies of fluorescently labeled P1 plasmids show that they move apart to become roughly evenly distributed throughout the length of the cell. This process is aided by the pairing and active separation of copies that lie close to each other (59). The properties of the ParA protein suggest that ParA forms dynamic gradients in the cell that direct plasmid movement.…”

Section: Type Ia Partition Systemsmentioning

confidence: 99%

Prevalence and Significance of Plasmid Maintenance Functions in the Virulence Plasmids of Pathogenic Bacteria

2011

Self Cite

View full text Add to dashboard Cite

Virulence functions of pathogenic bacteria are often encoded on large extrachromosomal plasmids. These plasmids are maintained at low copy number to reduce the metabolic burden on their host. Low-copy-number plasmids risk loss during cell division. This is countered by plasmid-encoded systems that ensure that each cell receives at least one plasmid copy. Plasmid replication and recombination can produce plasmid multimers that hinder plasmid segregation. These are removed by multimer resolution systems. Equitable distribution of the resulting monomers to daughter cells is ensured by plasmid partition systems that actively segregate plasmid copies to daughter cells in a process akin to mitosis in higher organisms. Any plasmid-free cells that still arise due to occasional failures of replication, multimer resolution, or partition are eliminated by plasmid-encoded postsegregational killing systems. Here we argue that all of these three systems are essential for the stable maintenance of large low-copy-number plasmids. Thus, they should be found on all large virulence plasmids. Where available, well-annotated sequences of virulence plasmids confirm this. Indeed, virulence plasmids often appear to contain more than one example conforming to each of the three system classes. Since these systems are essential for virulence, they can be regarded as ubiquitous virulence factors. As such, they should be informative in the search for new antibacterial agents and drug targets.Pathogenic bacteria differ from their harmless relatives in having genes for virulence factors that facilitate host invasion and infection. These factors either are encoded by the host chromosome or are carried on mobile genetic elements. The latter include transposons, viral prophages, and plasmids. Mobile elements provide an extensive library of potentially useful functions that can be readily adopted for the rapid adaptation of the bacterium to its environment. As these elements are acquired from other organisms in the biosphere, the bacterium has the potential to express a wide array of virulence-associated functions without the burden of carrying all the genetic information involved. Only those virulence factors required for the current adaptation need be carried. Since mobile elements are able to reassort the functions they carry by interaction with other elements in the biosphere, the variety and assortment of functions that can be acquired by transfer of an element are virtually unlimited.

show abstract

“…ParA/B systems are widespread among bacteria (6). For example, many low-copy-number plasmids encode a ParA/B system that distributes plasmid copies at regular intervals along the cell length (7)(8)(9)(10). This striking plasmid patterning ensures that division at midcell results in near-equal number of plasmids in each daughter cell.…”

mentioning

confidence: 99%

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

Surovtsev

Campos

Jacobs‐Wagner

2016

Proc. Natl. Acad. Sci. U.S.A.

121

View full text Add to dashboard Cite

Spatial ordering of macromolecular components inside cells is important for cellular physiology and replication. In bacteria, ParA/B systems are known to generate various intracellular patterns that underlie the transport and partitioning of low-copy-number cargos such as plasmids. ParA/B systems consist of ParA, an ATPase that dimerizes and binds DNA upon ATP binding, and ParB, a protein that binds the cargo and stimulates ParA ATPase activity. Inside cells, ParA is asymmetrically distributed, forming a propagating wave that is followed by the ParB-rich cargo. These correlated dynamics lead to cargo oscillation or equidistant spacing over the nucleoid depending on whether the cargo is in single or multiple copies. Currently, there is no model that explains how these different spatial patterns arise and relate to each other. Here, we test a simple DNArelay model that has no imposed asymmetry and that only considers the ParA/ParB biochemistry and the known fluctuating and elastic dynamics of chromosomal loci. Stochastic simulations with experimentally derived parameters demonstrate that this model is sufficient to reproduce the signature patterns of ParA/B systems: the propagating ParA gradient correlated with the cargo dynamics, the single-cargo oscillatory motion, and the multicargo equidistant patterning. Stochasticity of ATP hydrolysis breaks the initial symmetry in ParA distribution, resulting in imbalance of elastic force acting on the cargo. Our results may apply beyond ParA/B systems as they reveal how a minimal system of two players, one binding to DNA and the other modulating this binding, can transform directionally random DNA fluctuations into directed motion and intracellular patterning. intracellular patterning | active transport | ParA/B system | partitioning | mathematical model S patial patterns are omnipresent in biology, spanning a wide range of size scales and organizational levels. At the singlecell level, spatial patterns are readily apparent in the formation of protein gradients and the regular arrangement of cytoskeletal structures, macromolecular complexes, and organelles. Intracellular patterning serves important functions, as it provides a means for cells to organize their intracellular space, sense their geometry, and partition their cellular content (1-5). However, the mechanisms that drive intracellular patterning are often poorly understood.In this study, we aimed to understand how spatial patterns driven by bacterial ParA/B systems can arise within a small (micrometer-scale) intracellular space dominated by fluctuations and diffusion. ParA/B systems consist of only two proteins, ParA and ParB, that drive the transport and equipartitioning of lowcopy-number macromolecular complexes, often referred to as cargos. ParA/B systems are widespread among bacteria (6). For example, many low-copy-number plasmids encode a ParA/B system that distributes plasmid copies at regular intervals along the cell length (7-10). This striking plasmid patterning ensures that division at midcell results in ...

show abstract

P1 Plasmid Segregation: Accurate Redistribution by Dynamic Plasmid Pairing and Separation

Cited by 77 publications

References 37 publications

A three-dimensional ParF meshwork assembles through the nucleoid to mediate plasmid segregation

A three-dimensional ParF meshwork assembles through the nucleoid to mediate plasmid segregation

Prevalence and Significance of Plasmid Maintenance Functions in the Virulence Plasmids of Pathogenic Bacteria

DNA-relay mechanism is sufficient to explain ParA-dependent intracellular transport and patterning of single and multiple cargos

Contact Info

Product

Resources

About