Mixed Infections, Cryptic Diversity, and Vector-Borne Pathogens: Evidence from Polygenis Fleas and Bartonella Species

Abstract

Coinfections within hosts present opportunities for horizontal gene transfer between strains and competitive interactions between genotypes and thus can be a critical element of the lifestyles of pathogens. Bartonella spp. are Alphaproteobacteria that parasitize mammalian erythrocytes and endothelial cells. Their vectors are thought to be various biting arthropods, such as fleas, ticks, mites, and lice, and they are commonly cited as agents of various emerging diseases. Coinfections by different Bartonella strains and species can be common in mammals, but little is known about specificity and coinfections in arthropod vectors. We surveyed the rate of mixed infections of Bartonella in flea vectors (Polygenis gwyni) parasitizing cotton rats (Sigmodon hispidus) in which previous surveys indicated high rates of infection. We found that nearly all fleas (20 of 21) harbored one or more strains of Bartonella, with rates of coinfection approaching 90%. A strain previously identified as common in cotton rats was also common in their fleas. However, another common strain in cotton rats was absent from P. gwyni, while a rare cotton rat strain was quite common in P. gwyni. Surprisingly, some samples were also coinfected with a strain phylogenetically related to Bartonella clarridgeiae, which is typically associated with felids and ruminants. Finally, a locus (pap31) that is characteristically borne on phage in Bartonella was successfully sequenced from most samples. However, sequence diversity in pap31 was novel in the P. gwyni samples, relative to other Bartonella previously typed with pap31, emphasizing the likelihood of large reservoirs of cryptic diversity in natural populations of the pathogen.

Detection of multiple Bartonella species in digestive and reproductive tissues of fleas collected from sympatric mammals

“…These results suggest that fleas harbor richer Bartonella assemblages than their hosts, and that mammals may be exposed to a wider spectrum of Bartonella than those causing bacteremia. Abbot et al (2007) reported similar patterns of coinfection in rodent fleas and suggested that host specialization may account for mammal-Bartonella relationships. Bartonellae can 'jump' among host species (Jardine et al, 2005;Bai et al, 2007) and fleas have been implicated in facilitating such events (Bai et al, 2007).…”

The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas

“…Co-infection of hosts and vectors with more than one Bartonella species or genotype is a well-known phenomenon (Gurfield et al, 1997;Abbot et al, 2007;Breitschwerdt, 2008;Chan and Kosoy, 2010). However, questions relating to the composition, the potential interchange of bartonellae variants between hosts and vectors and the overall diversity of bartonellae in either environment are not fully clarified.…”

“…This genotype tended to dominate several flea-associated bartonellae infections (Table 2). With the development of the molecular techniques, the detection of concurrent multiple infections became more feasible (Abbot et al, 2007). The 454-pyrosequencing assay provided the benefit of receiving the maximal number of amplicons that could be detected in each sample (Dowd et al, 2008).…”

“…Although, only a few flea species were experimentally proven as competent vectors (Bown et al, 2004;Morick et al, 2011Morick et al, , 2013a, several Bartonella organisms have been detected in various flea species, suggesting their role as vectors and possibly as reservoirs (Loftis et al, 2006;Morick et al, 2010;Billeter et al, 2011;Deng et al, 2012). As reported in rodents, it has been documented that some fleas can carry more than one Bartonella species or variant (Abbot et al, 2007;Brinkerhoff et al, 2010). Moreover, some wholebacterial community analyses of fleas, performed by 16S rRNA gene characterization, have shown that Bartonella is one of the most abundant bacterial members of some flea species (Jones et al, 2008;Hawlena et al, 2013).…”

“…In fact, isolation methods together with modern genetic analyses had given only partial answers on the composition of Bartonella spp. coinfections and on the members hosted by a single infected individual (Abbot et al, 2007;Chan and Kosoy, 2010). However, deeper and more feasible tools for the detection of all co-existing members within a mixed infection are required.…”