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Run-off replication of host-adaptability genes is associated with gene transfer agents in the genome of mouse-infecting Bartonella grahamii.

Berglund EC, Frank AC, Calteau A, Vinnere Pettersson O, Granberg F, Eriksson AS, Näslund K, Holmberg M, Lindroos H, Andersson SG - PLoS Genet. (2009)

Bottom Line: Comparative genomics revealed that rodent-associated Bartonella species have higher copy numbers of genes for putative host-adaptability factors than the related human-specific pathogens.Because of the high concentration of gene clusters for host-adaptation proteins in the amplified region, and since the genes encoding the gene transfer agent and the phage origin are well conserved in Bartonella, we hypothesize that these systems are driven by selection.We propose that the coupling of run-off replication with gene transfer agents promotes diversification and rapid spread of host-adaptability factors, facilitating host shifts in Bartonella.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

ABSTRACT
The genus Bartonella comprises facultative intracellular bacteria adapted to mammals, including previously recognized and emerging human pathogens. We report the 2,341,328 bp genome sequence of Bartonella grahamii, one of the most prevalent Bartonella species in wild rodents. Comparative genomics revealed that rodent-associated Bartonella species have higher copy numbers of genes for putative host-adaptability factors than the related human-specific pathogens. Many of these gene clusters are located in a highly dynamic region of 461 kb. Using hybridization to a microarray designed for the B. grahamii genome, we observed a massive, putatively phage-derived run-off replication of this region. We also identified a novel gene transfer agent, which packages the bacterial genome, with an over-representation of the amplified DNA, in 14 kb pieces. This is the first observation associating the products of run-off replication with a gene transfer agent. Because of the high concentration of gene clusters for host-adaptation proteins in the amplified region, and since the genes encoding the gene transfer agent and the phage origin are well conserved in Bartonella, we hypothesize that these systems are driven by selection. We propose that the coupling of run-off replication with gene transfer agents promotes diversification and rapid spread of host-adaptability factors, facilitating host shifts in Bartonella.

Show MeSH
Phylogenetic analysis of genes for type V secretion systems.Phylogenetic trees of (A) autotransporters and (B) filamentous hemagglutinin. Bartonella genes are named with locus_tag (BARBAKC583 abbreviated as BB) and color-coded according to species: B. grahamii in red, B. tribocorum in blue, B. henselae in green, B. quintana in purple and B. bacilliformis in brown. After each B. grahamii gene, the genomic island in which the gene is located is indicated with numbers in circles. Branch lengths are according to maximum likelihood analysis and numbers represent bootstrap support values.
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pgen-1000546-g005: Phylogenetic analysis of genes for type V secretion systems.Phylogenetic trees of (A) autotransporters and (B) filamentous hemagglutinin. Bartonella genes are named with locus_tag (BARBAKC583 abbreviated as BB) and color-coded according to species: B. grahamii in red, B. tribocorum in blue, B. henselae in green, B. quintana in purple and B. bacilliformis in brown. After each B. grahamii gene, the genomic island in which the gene is located is indicated with numbers in circles. Branch lengths are according to maximum likelihood analysis and numbers represent bootstrap support values.

Mentions: The autotransporters are ubiquitously present in all five Bartonella genomes and their genomic locations suggest that they were ancestrally positioned in between core IIa and core IIb. A phylogeny of the transmembrane domain of the autotransporters revealed two distinct Bartonella clades, both of which contain all species (Figure 5A). B. bacilliformis represents the earliest diverging lineage in both clades, suggesting that the acquisition event(s) extends back to the root of the Bartonella tree. Due to a rearrangement in the rodent-associated lineage, the autotransporter genes in the high plasticity zone of these species are physically separated into two clusters with 5–7 genes in each cluster. In B. grahamii, these genes are located in BgGI 9 and BgGI 12 (Figure 4). Their physical separation corresponds to their phylogenetic divergence, suggesting that each of the two clusters have expanded and contracted independently through a series of tandem gene duplication and/or deletion events.


Run-off replication of host-adaptability genes is associated with gene transfer agents in the genome of mouse-infecting Bartonella grahamii.

Berglund EC, Frank AC, Calteau A, Vinnere Pettersson O, Granberg F, Eriksson AS, Näslund K, Holmberg M, Lindroos H, Andersson SG - PLoS Genet. (2009)

Phylogenetic analysis of genes for type V secretion systems.Phylogenetic trees of (A) autotransporters and (B) filamentous hemagglutinin. Bartonella genes are named with locus_tag (BARBAKC583 abbreviated as BB) and color-coded according to species: B. grahamii in red, B. tribocorum in blue, B. henselae in green, B. quintana in purple and B. bacilliformis in brown. After each B. grahamii gene, the genomic island in which the gene is located is indicated with numbers in circles. Branch lengths are according to maximum likelihood analysis and numbers represent bootstrap support values.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2697382&req=5

pgen-1000546-g005: Phylogenetic analysis of genes for type V secretion systems.Phylogenetic trees of (A) autotransporters and (B) filamentous hemagglutinin. Bartonella genes are named with locus_tag (BARBAKC583 abbreviated as BB) and color-coded according to species: B. grahamii in red, B. tribocorum in blue, B. henselae in green, B. quintana in purple and B. bacilliformis in brown. After each B. grahamii gene, the genomic island in which the gene is located is indicated with numbers in circles. Branch lengths are according to maximum likelihood analysis and numbers represent bootstrap support values.
Mentions: The autotransporters are ubiquitously present in all five Bartonella genomes and their genomic locations suggest that they were ancestrally positioned in between core IIa and core IIb. A phylogeny of the transmembrane domain of the autotransporters revealed two distinct Bartonella clades, both of which contain all species (Figure 5A). B. bacilliformis represents the earliest diverging lineage in both clades, suggesting that the acquisition event(s) extends back to the root of the Bartonella tree. Due to a rearrangement in the rodent-associated lineage, the autotransporter genes in the high plasticity zone of these species are physically separated into two clusters with 5–7 genes in each cluster. In B. grahamii, these genes are located in BgGI 9 and BgGI 12 (Figure 4). Their physical separation corresponds to their phylogenetic divergence, suggesting that each of the two clusters have expanded and contracted independently through a series of tandem gene duplication and/or deletion events.

Bottom Line: Comparative genomics revealed that rodent-associated Bartonella species have higher copy numbers of genes for putative host-adaptability factors than the related human-specific pathogens.Because of the high concentration of gene clusters for host-adaptation proteins in the amplified region, and since the genes encoding the gene transfer agent and the phage origin are well conserved in Bartonella, we hypothesize that these systems are driven by selection.We propose that the coupling of run-off replication with gene transfer agents promotes diversification and rapid spread of host-adaptability factors, facilitating host shifts in Bartonella.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden.

ABSTRACT
The genus Bartonella comprises facultative intracellular bacteria adapted to mammals, including previously recognized and emerging human pathogens. We report the 2,341,328 bp genome sequence of Bartonella grahamii, one of the most prevalent Bartonella species in wild rodents. Comparative genomics revealed that rodent-associated Bartonella species have higher copy numbers of genes for putative host-adaptability factors than the related human-specific pathogens. Many of these gene clusters are located in a highly dynamic region of 461 kb. Using hybridization to a microarray designed for the B. grahamii genome, we observed a massive, putatively phage-derived run-off replication of this region. We also identified a novel gene transfer agent, which packages the bacterial genome, with an over-representation of the amplified DNA, in 14 kb pieces. This is the first observation associating the products of run-off replication with a gene transfer agent. Because of the high concentration of gene clusters for host-adaptation proteins in the amplified region, and since the genes encoding the gene transfer agent and the phage origin are well conserved in Bartonella, we hypothesize that these systems are driven by selection. We propose that the coupling of run-off replication with gene transfer agents promotes diversification and rapid spread of host-adaptability factors, facilitating host shifts in Bartonella.

Show MeSH