Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors

Abstract

Bartonella spp. are facultative intracellular bacteria that cause characteristic hostrestricted hemotropic infections in mammals and are typically transmitted by blood-sucking arthropods. In the mammalian reservoir, these bacteria initially infect a yet unrecognized primary niche, which seeds organisms into the blood stream leading to the establishment of a long-lasting intra-erythrocytic bacteremia as the hall-mark of infection. Bacterial type IV secretion systems, which are supra-molecular transporters ancestrally related to bacterial conjugation systems, represent crucial pathogenicity factors that have contributed to a radial expansion of the Bartonella lineage in nature by facilitating adaptation to unique mammalian hosts. On the molecular level, the type IV secretion system VirB/VirD4 is known to translocate a cocktail of different effector proteins into host cells, which subvert multiple cellular functions to the benefit of the infecting pathogen. Furthermore, bacterial adhesins mediate a critical, early step in the pathogenesis of the bartonellae by binding to extracellular matrix components of host cells, which leads to firm bacterial adhesion to the cell surface as a prerequisite for the efficient translocation of type IV secretion effector proteins. The best-studied adhesins in bartonellae are the orthologous trimeric autotransporter adhesins, BadA in Bartonella henselae and the Vomp family in Bartonella quintana. Genetic diversity and strain variability also appear to enhance the ability of bartonellae to invade not only specific reservoir hosts, but also accidental hosts, as shown for B. henselae. Bartonellae have been identified in many different blood-sucking arthropods, in which they are typically found to cause extracellular infections of the mid-gut epithelium. Adaptation to specific vectors and reservoirs seems to be a common strategy of bartonellae for transmission and host diversity. However, knowledge regarding arthropod specificity/restriction, the mode of transmission, and the bacterial factors involved in arthropod infection and transmission is still limited.

Figure 1.

Model of the common infection cycle of Bartonella spp. in their revervoir host(s). The different infection stages in the mammalian reservoir have been resolved by tracking bacteria in the blood of experimentally infected animals (lined box), while little is known on the mode of infection of the blood-sucking arthropod vector (dashed-lined box); d.p.i. (days post-infection). Adapted from Schulein et al. [121].

Figure 2.

Phylogeny, arthropod vectors and mammalian hosts of the genus Bartonella and the distribution of type IV secretion systems. Left: Phylogenetic tree of the genus Bartonella based on multilocus sequence analysis (MLSA, [116]). Right: summary table of the host specificity and the presence and absence of loci encoding type IV secretion systems in the different Bartonella species. Adapted from Dehio [51].