Geographic distributions and vertebrate host specificity of genetic lineages of Borrelia burgdorferi
Date
2023
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Publisher
University of Delaware
Abstract
Characterizing the diversity of genes associated with virulence and transmission of a pathogen across the pathogen’s distribution can inform our understanding of host infection risk. Borrelia burgdorferi is a vector-borne bacterium that causes Lyme disease in humans and is common in the United States. The outer surface protein C (ospC) gene of B. burgdorferi exhibits substantial genetic variation across the pathogen’s distribution and plays a critical role in virulence and transmission in vertebrate hosts. In fact, B. burgdorferi infections that disseminate across host tissues in humans are associated with only a subset of ospC alleles. Delaware has a high incidence of Lyme disease, but the diversity of ospC in B. burgdorferi in the state has not been evaluated. We used PCR to amplify ospC in B. burgdorferi-infected blacklegged ticks (Ixodes scapularis) in sites statewide and used short-read sequencing to identify ospC alleles. B. burgdorferi prevalence in blacklegged ticks varied across sites, but not significantly so. We identified 15 previously characterized ospC alleles accounting for nearly all of the expected diversity of alleles across the sites as estimated using the Chao1 index. Nearly 40% of sequenced infections (23/58) had more than one ospC allele present suggesting mixed strain infections and the relative frequencies of alleles in single infections were positively correlated with their relative frequencies in mixed infections. Turnover of ospC alleles was positively related to distance between sites with closer sites having more similar allele compositions than more distant sites. This suggests a degree of B. burgdorferi dispersal limitation or habitat specialization. OspC alleles known to cause disseminated infections in humans were found at the highest frequencies across sites, corresponding to Delaware’s high incidence of Lyme disease. ☐ Negative interactions among pathogen genotypes during infection may affect overall transmission dynamics in multi-host systems. For example, specialist pathogens may limit the impact of generalists, which may become emerging infectious diseases. Borrelia burgdorferi, a bacterium that causes Lyme disease, is transmitted primarily among wildlife hosts and Ixodes ticks. Despite significant bacterial genetic diversity, most human infections are caused by bacteria with specific alleles of the outer surface protein C (ospC) gene (“human infectious alleles”; HIAs). We tested 272 individuals of 11 mammalian species for B. burgdorferi and sequenced ospC alleles. Multiple allele (“mixed”) infections were common in individuals of all species. HIAs were most common in mice (Peromyscus spp.) with only one HIA in a site with almost no mice. Chipmunks (Tamias striatus) were hosts of allele U, the only specialist. Surprisingly, while an unexpectedly large number of alleles were recovered from chipmunks, including HIAs, allele U was not found in mixed infections. These results are consistent with allele U excluding other alleles, perhaps through indirect host-immune mediated mechanisms, thereby reducing the capacity of chipmunks to act as reservoirs for HIAs. This suggests that specialized pathogens may be able to mitigate the infection risk of hosts they do not infect.
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Keywords
Host specificity, Ixodes scapularis, Lyme disease, ospC, Peromyscus, Tamias striatus