Distribution of centromere-like parS sites in bacteria: insights from comparative genomics

Abstract

Partitioning of low-copy-number plasmids to daughter cells often depends on ParA and ParB proteins acting on centromere-like parS sites. Similar chromosome-encoded par loci likely also contribute to chromosome segregation. Here, we used bioinformatic approaches to search for chromosomal parS sites in 400 prokaryotic genomes. Although the consensus sequence matrix used to search for parS sites was derived from two gram-positive species, putative parS sites were identified on the chromosomes of 69% of strains from all branches of bacteria. Strains that were not found to contain parS sites clustered among relatively few branches of the prokaryotic evolutionary tree. In the vast majority of cases, parS sites were identified in origin-proximal regions of chromosomes. The widespread conservation of parS sites across diverse bacteria suggests that par loci evolved very early in the evolution of bacterial chromosomes and that the absence of parS, parA, and/or parB in certain strains likely reflects the loss of one of more of these loci much later in evolution. Moreover, the highly conserved origin-proximal position of parS suggests par loci are primarily devoted to regulating processes that involve the origin region of bacterial chromosomes. In species containing multiple chromosomes, the parS sites found on secondary chromosomes diverge significantly from those found on their primary chromosomes, suggesting that chromosome segregation of multipartite genomes requires distinct replicon-specific par loci. Furthermore, parS sites on secondary chromosomes are not well conserved among different species, suggesting that the evolutionary histories of secondary chromosomes are more diverse than those of primary chromosomes.

FIG. 1.

WebLogos of putative parS site consensus sequences. A. Logos representing the 25 parS1 sites used to construct the S. coelicolor and B. subtilis consensus matrix and the 1,030 putative parS sites identified using this matrix. B. Logos representing the putative parS sites identified in secondary chromosomes using the indicated consensus matrices. The shaded boxes highlight conserved motifs.

FIG. 2.

ParABS profiles generally correlate with phylogenetic relationships. The phlyogenetic groupings are based on a phylogenetic tree available at the STRING website (http://string.embl.de/) (55). Phylogenetic phyla and classes are shown by the gray bars. Bact and Chlor correspond to the Bacteroidetes and Chlorobi phyla. The numbers in the S column correspond to the number(s) of parS sites contained by the strains in each branch; red cells denote that all strains in the branch contain a parS site; pink cells denote that only some strains in the branch contain a parS site; empty cells denote that no strain in the branch contains a putative parS site. In columns A and B, cells are shaded if all strains in the branch encode a putative ParA and ParB homologue, respectively; empty cells denote that no strain in the branch encodes a putative ParA or ParB. Asterisks denote that one strain in the branch encodes a ParA or ParB homologue. In column AB->S, light shading denotes branches in which all strains carry all three components within a region of the chromosome corresponding to 10% of its size. The dark shading denotes branches in which, in at least one strain, the distance between ParA or ParB and the nearest parS site is more than 10% of the replicon size. The numbers correspond to the range of these distances among the strains in that branch.

FIG. 3.

Distribution of the number of putative partitioning sites encoded per replicon. A. Sites identified on primary chromosomes identified using the S. coelicolor/B. subtilis consensus matrix. B. Sites identified on secondary chromosomes identified using parS2/IR consensus matrices.

FIG. 4.

Distribution of the locations of putative parS sites relative to their respective putative oriCs. Numbers denote the percentage of all putative sites. The top of each circle corresponds to the putative oriC. Each segment represents a region corresponding to 5% of the replicon size. Numbers denote the percentage of all sites located within the segment. A. Sites identified with the S. coelicolor/B. subtilis consensus matrix. B. Sites on secondary chromosomes identified with parS2/IR consensus matrices.

FIG. 5.

Venn diagram of ParABS profiles in the 400 strains analyzed. The numbers represent the percentage of the strains corresponding to each ParABS profile.