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Borrelia burgdorferi surface protein Lmp1 facilitates pathogen dissemination through ticks as studied by an artificial membrane feeding system.

ABSTRACT: In its natural infection cycle, the pathogen of Lyme borreliosis transits between a tick vector and a mammalian host. As relatively a minor fraction of spirochetes transits between the host and the vector precluding their reliable detection at early infection, artificial membrane feeders emerged as useful tools to study roles of spirochete proteins in pathogen entry, persistence, and exit through ticks. Here we report the development of a modified membrane feeder to study the role of a Borrelia burgdorferi surface protein called Lmp1 in spirochete transitions between the murine host and ticks. We show that our membrane feeder supports the blood meal engorgement process where ticks can acquire spirochetes from the feeder containing extremely low levels of pathogens (102 cells/ml of blood). Our data revealed that in comparison to wild-type spirochetes, lmp1 deletion mutants are significantly impaired for acquisition in naïve ticks as well as transmission from infected ticks. Taking together, our data suggest that Lmp1 plays an essential role in spirochete transitions between hosts and the vector. These studies also underscore the usefulness of artificial membrane feeding system as a valuable tool to study the role of B. burgdorferi gene-products in pathogen persistence in and passage through vector ticks.

SUBMITTER: Koci J

PROVIDER: S-EPMC5790009 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The controversy surrounding the potential impact of birds in spirochete transmission dynamics and their capacity to serve as a reservoir has existed for a long time. The majority of analyzed bird species are able to infect larval ticks with Borrelia. Dispersal of infected ticks due to bird migration is a key to the establishment of new foci of Lyme borreliosis. The dynamics of infection in birds supports the mixing of different species, the horizontal exchange of genetic information, and appearance of recombinant genotypes.Four Borrelia burgdorferi sensu lato strains were cultured from Ixodes minor larvae and four strains were isolated from Ixodes minor nymphs collected from a single Carolina Wren (Thryothorus ludovicianus). A multilocus sequence analysis that included 16S rRNA, a 5S-23S intergenic spacer region, a 16S-23S internal transcribed spacer, flagellin, p66, and ospC separated 8 strains into 3 distinct groups. Additional multilocus sequence typing of 8 housekeeping genes, clpA, clpX, nifS, pepX, pyrG, recG, rplB, and uvrA was used to resolve the taxonomic status of bird-associated strains.Results of analysis of 14 genes confirmed that the level of divergence among strains is significantly higher than what would be expected for strains within a single species. The presence of cross-species recombination was revealed: Borrelia burgdorferi sensu stricto housekeeping gene nifS was incorporated into homologous locus of strain, previously assigned to B. americana.Genetically diverse Borrelia strains are often found within the same tick or same vertebrate host, presenting a wide opportunity for genetic exchange. We report the cross-species recombination that led to incorporation of a housekeeping gene from the B. burgdorferi sensu stricto strain into a homologous locus of another bird-associated strain. Our results support the hypothesis that recombination maintains a majority of sequence polymorphism within Borrelia populations because of the re-assortment of pre-existing sequence variants. Even if our findings of broad genetic diversity among 8 strains cultured from ticks that fed on a single bird could be the exception rather than the rule, they support the theory that the diversity and evolution of LB spirochetes is driven mainly by the host.

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Borrelia burgdorferi surface protein Lmp1 facilitates pathogen dissemination through ticks as studied by an artificial membrane feeding system.

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