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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.

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Gene classifications in the Bartonella genomes.Diagram showing the number of genes that are predicted as vertically inherited (from closely related alpha-proteobacterial species), imported (horizontally transferred to the ancestor of Bartonella or more recently), Bartonella-specific (only present in Bartonella), and orphans (only present in one species) in the sequenced Bartonella genomes.
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pgen-1000546-g002: Gene classifications in the Bartonella genomes.Diagram showing the number of genes that are predicted as vertically inherited (from closely related alpha-proteobacterial species), imported (horizontally transferred to the ancestor of Bartonella or more recently), Bartonella-specific (only present in Bartonella), and orphans (only present in one species) in the sequenced Bartonella genomes.

Mentions: A prediction of the total amount of horizontally transferred genes by phylogenetic analysis (excluding plasmid genes and hypothetical genes solely identified in Bartonella) classified 729 imported genes (35%) in B. tribocorum and 457 such genes (26%) in B. grahamii (Figure 2). The human-specific pathogens B. quintana and B. bacilliformis have the smallest genomes with less than 125 imported genes each (∼10%). Only a few genes were initially identified in B. quintana that were absent or pseudogenized in B. henselae [3]. Our analysis shows that these genes have homologs in the rodent-associated Bartonella species; substantiating the hypothesis that B. quintana has evolved by lineage-specific losses with no novel gene acquisitions [3]. B. bacilliformis contains a few imported genes solely identified in this lineage, including 15 copies of a hypothetical gene that is also present in Leptospira interrogans. However, because there are no known close relatives of B. bacilliformis, we cannot infer the direction of evolution (loss or gain) of genes specific to this species.


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)

Gene classifications in the Bartonella genomes.Diagram showing the number of genes that are predicted as vertically inherited (from closely related alpha-proteobacterial species), imported (horizontally transferred to the ancestor of Bartonella or more recently), Bartonella-specific (only present in Bartonella), and orphans (only present in one species) in the sequenced Bartonella genomes.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000546-g002: Gene classifications in the Bartonella genomes.Diagram showing the number of genes that are predicted as vertically inherited (from closely related alpha-proteobacterial species), imported (horizontally transferred to the ancestor of Bartonella or more recently), Bartonella-specific (only present in Bartonella), and orphans (only present in one species) in the sequenced Bartonella genomes.
Mentions: A prediction of the total amount of horizontally transferred genes by phylogenetic analysis (excluding plasmid genes and hypothetical genes solely identified in Bartonella) classified 729 imported genes (35%) in B. tribocorum and 457 such genes (26%) in B. grahamii (Figure 2). The human-specific pathogens B. quintana and B. bacilliformis have the smallest genomes with less than 125 imported genes each (∼10%). Only a few genes were initially identified in B. quintana that were absent or pseudogenized in B. henselae [3]. Our analysis shows that these genes have homologs in the rodent-associated Bartonella species; substantiating the hypothesis that B. quintana has evolved by lineage-specific losses with no novel gene acquisitions [3]. B. bacilliformis contains a few imported genes solely identified in this lineage, including 15 copies of a hypothetical gene that is also present in Leptospira interrogans. However, because there are no known close relatives of B. bacilliformis, we cannot infer the direction of evolution (loss or gain) of genes specific to this species.

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