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Segrosome Complex Formation during DNA Trafficking in Bacterial Cell Division

View Article: PubMed Central - PubMed

ABSTRACT

Bacterial extrachromosomal DNAs often contribute to virulence in pathogenic organisms or facilitate adaptation to particular environments. The transmission of genetic information from one generation to the next requires sufficient partitioning of DNA molecules to ensure that at least one copy reaches each side of the division plane and is inherited by the daughter cells. Segregation of the bacterial chromosome occurs during or after replication and probably involves a strategy in which several protein complexes participate to modify the folding pattern and distribution first of the origin domain and then of the rest of the chromosome. Low-copy number plasmids rely on specialized partitioning systems, which in some cases use a mechanism that show striking similarity to eukaryotic DNA segregation. Overall, there have been multiple systems implicated in the dynamic transport of DNA cargo to a new cellular position during the cell cycle but most seem to share a common initial DNA partitioning step, involving the formation of a nucleoprotein complex called the segrosome. The particular features and complex topologies of individual segrosomes depend on both the nature of the DNA binding protein involved and on the recognized centromeric DNA sequence, both of which vary across systems. The combination of in vivo and in vitro approaches, with structural biology has significantly furthered our understanding of the mechanisms underlying DNA trafficking in bacteria. Here, I discuss recent advances and the molecular details of the DNA segregation machinery, focusing on the formation of the segrosome complex.

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Structural comparison of CBPs involved in segrosome assembly by wrapping. (A) Type II partition systems. Structure of ParR dimer (left), showing topology and the RHH motif; DNA changes upon ParR binding (middle), with enlargement of the DNA major groove; and formation of the the segrosome complex by DNA wrapping of the ParR super-helical oligomer (right), leaving the ParR C-terminal tail in the helix inside. (B) Type III partition systems. Structure of TubR dimer (left), showing topology and the HTH motif; the TubR-DNA binding mechanism (middle), in which the HTH makes contacts with the DNA major groove and the wing forms contacts with the minor groove; and putative filamentous vs. helical segrosome complexes (right), according to two crystal packing arrangements. (C) Type Ib partition systems. Structures of ParG and ω dimers (left), showing the RHH motif and the flexible N-terminal domain, and protein binding to direct and inverted repeats in equivalent ways (right).
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Figure 2: Structural comparison of CBPs involved in segrosome assembly by wrapping. (A) Type II partition systems. Structure of ParR dimer (left), showing topology and the RHH motif; DNA changes upon ParR binding (middle), with enlargement of the DNA major groove; and formation of the the segrosome complex by DNA wrapping of the ParR super-helical oligomer (right), leaving the ParR C-terminal tail in the helix inside. (B) Type III partition systems. Structure of TubR dimer (left), showing topology and the HTH motif; the TubR-DNA binding mechanism (middle), in which the HTH makes contacts with the DNA major groove and the wing forms contacts with the minor groove; and putative filamentous vs. helical segrosome complexes (right), according to two crystal packing arrangements. (C) Type Ib partition systems. Structures of ParG and ω dimers (left), showing the RHH motif and the flexible N-terminal domain, and protein binding to direct and inverted repeats in equivalent ways (right).

Mentions: Surprisingly, the arrangement of the components in Type Ib systems is the only common aspect shared with the aforementioned systems. The interactions between their main components are different, and so may be the segregation mechanism. The centromere site localizes upstream of the par operon and consists of direct and inverted repeats. However, in plasmid pCXC100 the centromeric site contains only direct repeats (Yin et al., 2006; Huang et al., 2011). The CBPs, which also functions as repressors (Carmelo et al., 2005; Weihofen et al., 2006) are small proteins that share the arrangement into N- and C-terminal domains (Figure 2C). The N-terminal domain, which shows a highly divergent sequence, is flexible and unstructured, and includes a conserved arginine finger that has been implicated in the activation of ATP hydrolysis in the motor protein (Barilla et al., 2007). The C-terminal domain topology is β1-α1-α2 and includes a ribbon-helix-helix (RHH) DNA-binding motif (Murayama et al., 2001; Golovanov et al., 2003; Huang et al., 2011). The β1 strand from two different molecules pairs into an antiparallel β-ribbon, meaning that these CBPs are also present as dimers in solution (Barilla and Hayes, 2003; Golovanov et al., 2003).


Segrosome Complex Formation during DNA Trafficking in Bacterial Cell Division
Structural comparison of CBPs involved in segrosome assembly by wrapping. (A) Type II partition systems. Structure of ParR dimer (left), showing topology and the RHH motif; DNA changes upon ParR binding (middle), with enlargement of the DNA major groove; and formation of the the segrosome complex by DNA wrapping of the ParR super-helical oligomer (right), leaving the ParR C-terminal tail in the helix inside. (B) Type III partition systems. Structure of TubR dimer (left), showing topology and the HTH motif; the TubR-DNA binding mechanism (middle), in which the HTH makes contacts with the DNA major groove and the wing forms contacts with the minor groove; and putative filamentous vs. helical segrosome complexes (right), according to two crystal packing arrangements. (C) Type Ib partition systems. Structures of ParG and ω dimers (left), showing the RHH motif and the flexible N-terminal domain, and protein binding to direct and inverted repeats in equivalent ways (right).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5016525&req=5

Figure 2: Structural comparison of CBPs involved in segrosome assembly by wrapping. (A) Type II partition systems. Structure of ParR dimer (left), showing topology and the RHH motif; DNA changes upon ParR binding (middle), with enlargement of the DNA major groove; and formation of the the segrosome complex by DNA wrapping of the ParR super-helical oligomer (right), leaving the ParR C-terminal tail in the helix inside. (B) Type III partition systems. Structure of TubR dimer (left), showing topology and the HTH motif; the TubR-DNA binding mechanism (middle), in which the HTH makes contacts with the DNA major groove and the wing forms contacts with the minor groove; and putative filamentous vs. helical segrosome complexes (right), according to two crystal packing arrangements. (C) Type Ib partition systems. Structures of ParG and ω dimers (left), showing the RHH motif and the flexible N-terminal domain, and protein binding to direct and inverted repeats in equivalent ways (right).
Mentions: Surprisingly, the arrangement of the components in Type Ib systems is the only common aspect shared with the aforementioned systems. The interactions between their main components are different, and so may be the segregation mechanism. The centromere site localizes upstream of the par operon and consists of direct and inverted repeats. However, in plasmid pCXC100 the centromeric site contains only direct repeats (Yin et al., 2006; Huang et al., 2011). The CBPs, which also functions as repressors (Carmelo et al., 2005; Weihofen et al., 2006) are small proteins that share the arrangement into N- and C-terminal domains (Figure 2C). The N-terminal domain, which shows a highly divergent sequence, is flexible and unstructured, and includes a conserved arginine finger that has been implicated in the activation of ATP hydrolysis in the motor protein (Barilla et al., 2007). The C-terminal domain topology is β1-α1-α2 and includes a ribbon-helix-helix (RHH) DNA-binding motif (Murayama et al., 2001; Golovanov et al., 2003; Huang et al., 2011). The β1 strand from two different molecules pairs into an antiparallel β-ribbon, meaning that these CBPs are also present as dimers in solution (Barilla and Hayes, 2003; Golovanov et al., 2003).

View Article: PubMed Central - PubMed

ABSTRACT

Bacterial extrachromosomal DNAs often contribute to virulence in pathogenic organisms or facilitate adaptation to particular environments. The transmission of genetic information from one generation to the next requires sufficient partitioning of DNA molecules to ensure that at least one copy reaches each side of the division plane and is inherited by the daughter cells. Segregation of the bacterial chromosome occurs during or after replication and probably involves a strategy in which several protein complexes participate to modify the folding pattern and distribution first of the origin domain and then of the rest of the chromosome. Low-copy number plasmids rely on specialized partitioning systems, which in some cases use a mechanism that show striking similarity to eukaryotic DNA segregation. Overall, there have been multiple systems implicated in the dynamic transport of DNA cargo to a new cellular position during the cell cycle but most seem to share a common initial DNA partitioning step, involving the formation of a nucleoprotein complex called the segrosome. The particular features and complex topologies of individual segrosomes depend on both the nature of the DNA binding protein involved and on the recognized centromeric DNA sequence, both of which vary across systems. The combination of in vivo and in vitro approaches, with structural biology has significantly furthered our understanding of the mechanisms underlying DNA trafficking in bacteria. Here, I discuss recent advances and the molecular details of the DNA segregation machinery, focusing on the formation of the segrosome complex.

No MeSH data available.


Related in: MedlinePlus