The louse-borne human pathogen Bartonella quintana is a genomic derivative of the zoonotic agent Bartonella henselae

Abstract

We present the complete genomes of two human pathogens, Bartonella quintana (1,581,384 bp) and Bartonella henselae (1,931,047 bp). The two pathogens maintain several similarities in being transmitted by insect vectors, using mammalian reservoirs, infecting similar cell types (endothelial cells and erythrocytes) and causing vasculoproliferative changes in immunocompromised hosts. A primary difference between the two pathogens is their reservoir ecology. Whereas B. quintana is a specialist, using only the human as a reservoir, B. henselae is more promiscuous and is frequently isolated from both cats and humans. Genome comparison elucidated a high degree of overall similarity with major differences being B. henselae specific genomic islands coding for filamentous hemagglutinin, and evidence of extensive genome reduction in B. quintana, reminiscent of that found in Rickettsia prowazekii. Both genomes are reduced versions of chromosome I from the highly related pathogen Brucella melitensis. Flanked by two rRNA operons is a segment with similarity to genes located on chromosome II of B. melitensis, suggesting that it was acquired by integration of megareplicon DNA in a common ancestor of the two Bartonella species. Comparisons of the vector-host ecology of these organisms suggest that the utilization of host-restricted vectors is associated with accelerated rates of genome degradation and may explain why human pathogens transmitted by specialist vectors are outnumbered by zoonotic agents, which use vectors of broad host ranges.

A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana

“…There are several mechanisms by which functional vomp genes could be restored in the setting of gene deletion, including gene duplication or recombination either with exogenously acquired B. quintana DNA or with vomp gene fragments at other locations on the chromosomal DNA. The newly released genome sequence for the B. quintana strain Toulouse reveals vomp gene fragments downstream of vompC: one that is tandemly arranged (similar to the fragment that we have identified in JK-31) and one that is inverted (31). In addition, this strain has only three complete vomp genes: vompD, vompC, and between these two genes, a gene that is a mosaic of vompA, vompB, and vompC, potentially representing some recombination event(s).…”

Bartonella henselae exists as a mosaic of different genetic variants in the infected host

“…Furthermore, it is possible that a distinct variant may eventually overgrow the other variants within the community of an isolate under certain environmental conditions, giving rise to a high-passage isolate with different genetic or antigenic properties than the original one. This could explain the observation of several investigators who found that the copy of the Houston-1 isolate used in their laboratory was different from the previously described Houston-1 isolate (Alsmark et al, 2004;Kyme et al, 2003;Riess et al, 2007). Further studies are required to test this hypothesis, e.g.…”

“…Kyme et al (2003) demonstrated that B. henselae may undergo phase variation in vitro, a process that is characterized by the emergence of antigenic variants. More recently, the complete genome of B. henselae was found to contain several regions with numerous short repeats in tandem that are prone to rearrangement and may be implicated in phase variation (Alsmark et al, 2004).…”

The α-proteobacteria: the Darwin finches of the bacterial world

“…The auxiliary replicons may also integrate into the main chromosome (figure 2b), as observed in Bartonella (Alsmark et al 2004) and Bradyrhizobium (Viprey et al 2000). Such integration events serve to stabilize the auxiliary gene pool, thereby preventing its loss from the population.…”