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Chapter 7 : Chromosome Replication and Segregation

Authors: Katherine P. Lemon, Shigeki Moriya, Naotake Ogasawara, Alan D. Grossman
Content Type: Monograph
Publication Year: 2002

Category: Bacterial Pathogenesis

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Abstract:

This chapter reviews our current understanding of bacterial DNA replication and chromosome partitioning in and makes comparisons to and other organisms where appropriate. Bacterial chromosome replication initiates once per cell division cycle in response to a signal that is tightly coupled to cell mass. Although the helicase function of DnaC has not yet been confirmed biochemically, two types of (TS) mutations, defective in initiation and elongation, map to . Strong interaction between the helicase and the primase has been demonstrated in . The current understanding of bacterial chromosome partitioning can be simplified into three steps: (i) origin region separation and repositioning, (ii) overall chromosome organization and compaction, and (iii) terminus region separation. This final step includes chromosome decatenation, chromosome dimer-to-monomer resolution when necessary, and movement of the termini to either side of midcell before completion of medial division. The structural maintenance of chromosomes (SMC) protein family is well conserved and is important for chromosome segregation in bacteria, archaea, and eukaryotes. Both and have proteins that appear to be involved in postseptational chromosome partitioning. These proteins, SpoIIIE and FtsK, respectively, have domains that are homologous to the DNA translocation domains of proteins involved in conjugative plasmid transfer. In and , SMC functions in chromosome partitioning presumably by affecting chromosome organization and compaction. All organisms seem to have proteins that contribute to chromosome folding and compaction.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7

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Chromosome Replication and Segregation
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Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
/content/10.1128/9781555817992.chap7.fig7-1
FIGURE 1

Simplified cartoon of the bacterial cell cycle and chromosome orientation. The chromosome is indicated by a thin oval inside the cell. The origin of replication () is indicated by a small gray circle, and the terminus of replication () is indicated by a gray square. The replisome is indicated by two triangles, one for each replication fork that initiates from . In this model, replication initiates at or near midcell, the origins rapidly separate, replication continues as the newly replicated DNA is refolded (in part by Smc), and copies separate from each other. The cell division machinery assembles at midcell, and cells divide. This is simplified, because at rapid growth rates, newborn cells have a partly duplicated chromosome and the origin regions have already duplicated and separated to the cell quarters.

10.1128/9781555817992/fig7-1_thmb.gif
10.1128/9781555817992/fig7-1.gif
Image of FIGURE 1
FIGURE 1

Simplified cartoon of the bacterial cell cycle and chromosome orientation. The chromosome is indicated by a thin oval inside the cell. The origin of replication () is indicated by a small gray circle, and the terminus of replication () is indicated by a gray square. The replisome is indicated by two triangles, one for each replication fork that initiates from . In this model, replication initiates at or near midcell, the origins rapidly separate, replication continues as the newly replicated DNA is refolded (in part by Smc), and copies separate from each other. The cell division machinery assembles at midcell, and cells divide. This is simplified, because at rapid growth rates, newborn cells have a partly duplicated chromosome and the origin regions have already duplicated and separated to the cell quarters.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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FIGURE 2

Model of initiation mechanism of chromosome replication. The gene constitutes an operon with ( ). DnaA boxes exist in two noncoding regions upstream and downstream of , where DnaA actually binds ( ). The operon is probably expressed after initiation of replication ( ) and is autoregulated by DnaA ( ). Thus, DnaA newly synthesized after initiation would stop its transcription. Two DnaA box clusters are required for initiation of replication in vivo (shown as , autonomously replicating sequence) ( ), and the regions form a loop mediated by DnaA in vitro ( ). It is unclear whether the loop is formed only at the time of initiation. This loop formation opens double-stranded DNA locally at an AT-rich sequence between and ( ), consistent with in vivo observations that plasmid and chromosome replication start at this non-coding region ( ). DnaB, DnaD, and Dnal are probably components of a primosome ( ) and thus play roles for loading the DnaC helicase into the unwound region. DnaD interacts with DnaA ( ), but the role of the interaction is still unclear. DnaB exhibits single-stranded DNA-binding activity ( ) and forms an oligomer ( ), similar to DnaC helicase loader. However, DnaB did not interact with DnaA, DnaC, DnaD, or Dnal by the yeast two-hybrid assay ( ). Its precise role is still obscure. Dnal interacted strongly with the DnaC helicase ( ), indicating that it acts as a component of the helicase loading system. Once the helicase is loaded into , primase (DnaG) and τ subunit (DnaX) of DNA polymerase III are assembled by protein-protein interaction followed by formation of the replisome on .

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10.1128/9781555817992/fig7-2.gif
Image of FIGURE 2
FIGURE 2

Model of initiation mechanism of chromosome replication. The gene constitutes an operon with ( ). DnaA boxes exist in two noncoding regions upstream and downstream of , where DnaA actually binds ( ). The operon is probably expressed after initiation of replication ( ) and is autoregulated by DnaA ( ). Thus, DnaA newly synthesized after initiation would stop its transcription. Two DnaA box clusters are required for initiation of replication in vivo (shown as , autonomously replicating sequence) ( ), and the regions form a loop mediated by DnaA in vitro ( ). It is unclear whether the loop is formed only at the time of initiation. This loop formation opens double-stranded DNA locally at an AT-rich sequence between and ( ), consistent with in vivo observations that plasmid and chromosome replication start at this non-coding region ( ). DnaB, DnaD, and Dnal are probably components of a primosome ( ) and thus play roles for loading the DnaC helicase into the unwound region. DnaD interacts with DnaA ( ), but the role of the interaction is still unclear. DnaB exhibits single-stranded DNA-binding activity ( ) and forms an oligomer ( ), similar to DnaC helicase loader. However, DnaB did not interact with DnaA, DnaC, DnaD, or Dnal by the yeast two-hybrid assay ( ). Its precise role is still obscure. Dnal interacted strongly with the DnaC helicase ( ), indicating that it acts as a component of the helicase loading system. Once the helicase is loaded into , primase (DnaG) and τ subunit (DnaX) of DNA polymerase III are assembled by protein-protein interaction followed by formation of the replisome on .

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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FIGURE 3

Model of proteins present at the replication fork of

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Image of FIGURE 3
FIGURE 3

Model of proteins present at the replication fork of

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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FIGURE 4

Spo0J binding sites on the chromosome. is at 0°/360° on the circular chromosome. The eight known sites ( ) are indicated.

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10.1128/9781555817992/fig7-4.gif
Image of FIGURE 4
FIGURE 4

Spo0J binding sites on the chromosome. is at 0°/360° on the circular chromosome. The eight known sites ( ) are indicated.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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FIGURE 5

Model of SMC. SMC is an antiparallel homodimer with two long coiled-coil regions separated by a flexible hinge ( ).

10.1128/9781555817992/fig7-5_thmb.gif
10.1128/9781555817992/fig7-5.gif
Image of FIGURE 5
FIGURE 5

Model of SMC. SMC is an antiparallel homodimer with two long coiled-coil regions separated by a flexible hinge ( ).

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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FIGURE 6

Chromosome partitioning events specific to the terminus region. (A) Chromosome decatenation. (B) When necessary, a site-specific recombination resolves a chromosome dimer (left) to two monomers. (C) Model for SpoIIIE (or FtsK) movement of trapped chromosome out of the division septum.

10.1128/9781555817992/fig7-6_thmb.gif
10.1128/9781555817992/fig7-6.gif
Image of FIGURE 6
FIGURE 6

Chromosome partitioning events specific to the terminus region. (A) Chromosome decatenation. (B) When necessary, a site-specific recombination resolves a chromosome dimer (left) to two monomers. (C) Model for SpoIIIE (or FtsK) movement of trapped chromosome out of the division septum.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
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Tables

Chromosome Replication and Segregation
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Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
/content/10.1128/9781555817992.chap7.tab7-1
TABLE 1

genes involved in chromosomal DNA replication

The numbers indicate nucleotide positions of each gene (coding region) on the whole genome. To the left and right of the hyphen are positions of the first and last letters of start and stop codons, respectively. (See http://bacillus.genome.ad.jp/ or http://genolist.pasteur.fr/SubtiList/)

Personal communication from S.D. Ehrlich.

and constitute an operon ( ). is a member of the operon ( ). and belong to a putative operon ( ).

and , γ subunit is also produced from the gene by translational frameshifting and transcriptional slippage, respectively ( ). The existence of γ has not yet been confirmed in .

The core of DNA polymerase III consists of α, є, and θ subunits ( ). In , the activity of proofreading exonuclease (є) is included in the α subunit, and no homologs of θ are found.

10.1128/9781555817992/tab7-1_thmb.gif
10.1128/9781555817992/tab7-1.gif
Generic image for table
TABLE 1

genes involved in chromosomal DNA replication

The numbers indicate nucleotide positions of each gene (coding region) on the whole genome. To the left and right of the hyphen are positions of the first and last letters of start and stop codons, respectively. (See http://bacillus.genome.ad.jp/ or http://genolist.pasteur.fr/SubtiList/)

Personal communication from S.D. Ehrlich.

and constitute an operon ( ). is a member of the operon ( ). and belong to a putative operon ( ).

and , γ subunit is also produced from the gene by translational frameshifting and transcriptional slippage, respectively ( ). The existence of γ has not yet been confirmed in .

The core of DNA polymerase III consists of α, є, and θ subunits ( ). In , the activity of proofreading exonuclease (є) is included in the α subunit, and no homologs of θ are found.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7
/content/10.1128/9781555817992.chap7.tab7-2
TABLE 2

Orthologous proteins involved in chromosome replication in gram-positive bacteria and

Orthologous genes were searched by BLAST 2.0 (Advanced) and specialized BLAST to Microbial Genomes (finished and unfinished) at the National Center for Biotechnology Information website using proteins as query. Where there were no orthologs in , proteins were used as query. The amino acid sequences of query proteins were obtained from http://bacillus.genome.ad.jp/ and http://dna.aist-nara.ac.jp/ecoli/ for and , respectively. Orthologous genes having alignment scores of >100 are listed except where noted. In , , , and , the presence of the orthologs is shown as “+” because the gene names were not available in the databases. When orthologs were not found but the genome sequencing had not yet been completed, the columns remain blank. Genome sequencing has finished in , but annotation of genes has not been done. Therefore, when orthologs are not detected, “−” is given in such columns.

Abbreviations of strains, with references: , ; , ; , ( ); , ; , ( ); , ( ); , ( ); , ; , ; , ( ); , ( ).

Alignment score, 30–50.

BLAST search (tblastn) identified a homologous gene here, but no coding sequence is assigned in the database.

Alignment score, 50–100.

In this organism, δ has been recently found, and a τδδ′ complex (without γ) actually acts as a clamp loader ( ).

These genes are named in their original databases but are renamed in this table.

10.1128/9781555817992/tab7-2_thmb.gif
10.1128/9781555817992/tab7-2.gif
Generic image for table
TABLE 2

Orthologous proteins involved in chromosome replication in gram-positive bacteria and

Orthologous genes were searched by BLAST 2.0 (Advanced) and specialized BLAST to Microbial Genomes (finished and unfinished) at the National Center for Biotechnology Information website using proteins as query. Where there were no orthologs in , proteins were used as query. The amino acid sequences of query proteins were obtained from http://bacillus.genome.ad.jp/ and http://dna.aist-nara.ac.jp/ecoli/ for and , respectively. Orthologous genes having alignment scores of >100 are listed except where noted. In , , , and , the presence of the orthologs is shown as “+” because the gene names were not available in the databases. When orthologs were not found but the genome sequencing had not yet been completed, the columns remain blank. Genome sequencing has finished in , but annotation of genes has not been done. Therefore, when orthologs are not detected, “−” is given in such columns.

Abbreviations of strains, with references: , ; , ; , ( ); , ; , ( ); , ( ); , ( ); , ; , ; , ( ); , ( ).

Alignment score, 30–50.

BLAST search (tblastn) identified a homologous gene here, but no coding sequence is assigned in the database.

Alignment score, 50–100.

In this organism, δ has been recently found, and a τδδ′ complex (without γ) actually acts as a clamp loader ( ).

These genes are named in their original databases but are renamed in this table.

Citation: Lemon K, Moriya S, Ogasawara N, Grossman A. 2002. Chromosome Replication and Segregation, p 73-86. In Sonenshein A, Losick R, Hoch J (ed), and Its Closest Relatives. ASM Press, Washington, DC. doi: 10.1128/9781555817992.ch7

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