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Expanding our view of Bartonella and its hosts: Bartonella in nest ectoparasites and their migratory avian hosts.

ABSTRACT: BACKGROUND:Bartonella is a genus of Gram-negative facultative intracellular Alphaproteobacteria of public health importance. Although they are known to mainly infect mammalian hosts with some blood-feeding arthropods having been confirmed as vectors, there is some evidence of Bartonella association with non-mammalian hosts including birds. METHODS:Here we used high-throughput sequencing of 16S rRNA and Sanger sequencing of the citrate synthase (gltA) genes to test for the presence of Bartonellaceae in the blood of three migratory cavity nesting bird species, purple martins (Progne subis), tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis) and their most prevalent and abundant nest ectoparasites, Dermanyssus prognephilus (mite), Ceratophyllus idius (flea) and Protocalliphora sialia (bird blow fly larva). We constructed maximum likelihood phylogenetic trees to verify the placement of the resulting sequences in the Bartonellaceae. RESULTS:We found evidence of Bartonella in all three bird species and all three arthropod species tested. We report multiple instances of identical Bartonella sequences in both birds and parasites, leading to the likely hypothesis that these ectoparasites are potential vectors of Bartonella. Our phylogenetic analysis suggests that 'avian Bartonella' may form its own sub-clade within the genus Bartonella. CONCLUSIONS:To the best of our knowledge, we provide the first confirmation of overlapping Bartonella strains among bird hosts and various species of nest-associated ectoparasites from the same system, suggesting a possible Bartonella host-vector relationship between these arthropods and a non-mammalian host. Our study adds to the growing appreciation of the Bartonellaceae as a phylogenetically diverse group with a wide range of hosts.

SUBMITTER: Williams HM

PROVIDER: S-EPMC6954622 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundTicks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations. Ticks may have detrimental effects on the health state of their avian hosts, which can be either directly caused by blood-draining or mediated by microbial pathogens transmitted during the blood meal. Indeed, ticks host complex microbial communities, including bacterial pathogens and symbionts. Midichloria bacteria (Rickettsiales) are widespread tick endosymbionts that can be transmitted to vertebrate hosts during the tick bite, inducing an antibody response. Their actual role as infectious/pathogenic agents is, however, unclear.MethodsWe screened for Midichloria DNA African ticks and blood samples collected from trans-Saharan migratory songbirds at their arrival in Europe during spring migration.ResultsTick infestation rate was 5.7%, with most ticks belonging to the Hyalomma marginatum species complex. Over 90% of Hyalomma ticks harboured DNA of Midichloria bacteria belonging to the monophylum associated with ticks. Midichloria DNA was detected in 43% of blood samples of avian hosts. Tick-infested adult birds were significantly more likely to test positive to the presence of Midichloria DNA than non-infested adults and second-year individuals, suggesting a long-term persistence of these bacteria within avian hosts. Tick parasitism was associated with a significantly delayed timing of spring migration of avian hosts but had no significant effects on body condition, whereas blood Midichloria DNA presence negatively affected fat deposits of tick-infested avian hosts.ConclusionsOur results show that ticks effectively transfer Midichloria bacteria to avian hosts, supporting the hypothesis that they are infectious to vertebrates. Bird infection likely enhances the horizontal spread of these bacteria across haematophagous ectoparasite populations. Moreover, we showed that Midichloria and tick parasitism have detrimental non-independent effects on avian host health during migration, highlighting the complexity of interactions involving ticks, their vertebrate hosts, and tick-borne bacteria.

Dataset Information

Expanding our view of Bartonella and its hosts: Bartonella in nest ectoparasites and their migratory avian hosts.

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