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Role of Phages and Islands in the Evolution of Bartonella

Comparisons of B. henselae and B. quintana have revealed that most of the differences between them are related to the B. henselae prophage. The largest genomic island unique to B. henselae shares extensive sequence homology and possibly integration mechanisms with the prophage, and many of the B. henselae islets carry remnants of what appears to be the same phage. Even the two B. quintana-specific genes with assigned function are located adjacent to a phage and a tRNA gene respectively. All these phage remnants along with evidence of horizontal transfer possibly performed by the phage suggest that the phage has played a crucial role in the evolution of Bartonella.

One of the most striking features of the prophage and the genomic islands is their high degree of repetition. This redundancy could be the result of multiple phage integration events, or intragenomic duplication or recombination events, or a combination of the above. Duplication of phage genes may be beneficial for the phage or its host; slightly different copies of the fhaC/hecB-fhaB cluster could for instance be used in the colonization of different bacterial species, vectors, or host cells, or in different stages of infection. It is possible that the prophage proteins regulate the transcription of the virulence genes located on the islands, which would imply a selective advantage associated with their overexpression.

13.6 The Chromosome II-Like Segment in Bartonella | 291

The presence of both a complete prophage and heavily degraded integrase copies suggests on the one hand that the phage could still be active, and on the other hand that the phage association is old and could have contributed to diversification of the whole Bartonella genus. Since the variation at the sequence level between Bartonella species is low, it is likely that the genetic basis for differences in host preference and pathogenicity between them lies in the presence or absence of clusters of virulence genes, like the islands in B. henselae.

It is possible that phages are involved not only in the diversification of Bartonella species, but also in their evolution from the common ancestor of Brucella and Bartonella and, before that, from plant pathogens and symbionts. Considering the whole group of a-proteobacteria, it is clear that much of the diversity in gene content is due to the presence of highly dynamic auxiliary replicons. In the a-pro-teobacteria, auxiliary replicons are much less conserved than main chromosomes, suggesting that they are more amenable to influx of genetic material. It is possible that the acquisition of the prophage and its contributed gene sets, which potentially was an important step in the formation of the Bartonella genus, was mediated by an auxiliary replicon which was later integrated in the main chromosome. In plant-associated bacteria, genes involved in host interactions have been found located at mobile and unstable genetic elements [70]. Likewise, in Bartonella, many species-specific genes potentially involved in interaction with the animal host are located in a region that may have originated as an integrated auxiliary replicon.

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