Diversity and host specificity of Borrelia burgdorferi's outer surface protein C (ospC) alleles in synanthropic mammals, with a notable ospC allele U absence from mixed infections

Interactions among pathogen genotypes that vary in host specificity may affect overall transmission dynamics in multi-host systems. Borrelia burgdorferi, a bacterium that causes Lyme disease, is typically transmitted among wildlife by Ixodes ticks. Despite the existence of many alleles of B. burgdorferi’s sensu stricto outer surface protein C (ospC) gene, most human infections are caused by a small number of ospC alleles [“human infectious alleles” (HIAs)], suggesting variation in host specificity associated with ospC. To characterize the wildlife host association of B. burgdorferi’s ospC alleles, we used metagenomics to sequence ospC alleles from 68 infected individuals belonging to eight mammalian species trapped at three sites in suburban New Brunswick, New Jersey (USA). We found that multiple allele (“mixed”) infections were common. HIAs were most common in mice (Peromyscus spp.) and only one HIA was detected at a site where mice were rarely captured. OspC allele U was exclusively found in chipmunks (Tamias striatus), and although a significant number of different alleles were observed in chipmunks, including HIAs, allele U never co-occurred with other alleles in mixed infections. Our results suggest that allele U may be excluding other alleles, thereby reducing the capacity of chipmunks to act as reservoirs for HIAs.

宿主特异性存在差异的病原体基因型之间的相互作用，可能会影响多宿主系统中的整体传播动态。引发莱姆病（Lyme disease）的伯氏疏螺旋体（Borrelia burgdorferi）通常经由硬蜱（Ixodes ticks）在野生动物间传播。尽管严格意义上的伯氏疏螺旋体（B. burgdorferi sensu stricto）的外表面蛋白C（outer surface protein C, ospC）基因存在众多等位基因，但绝大多数人类感染均由少数几种ospC等位基因——即“人类感染性等位基因（human infectious alleles, HIAs）”——所引发，这表明ospC基因与宿主特异性差异存在关联。为了阐明伯氏疏螺旋体ospC等位基因与野生宿主的关联，我们利用宏基因组学（metagenomics）技术，对来自美国新泽西州新不伦瑞克郊区3个采样点、捕获的8种哺乳动物共68名感染个体体内的ospC等位基因进行了测序。研究发现，多等位基因（即“混合”）感染现象较为普遍。人类感染性等位基因（HIAs）在鹿鼠属（Peromyscus spp.）小鼠中最为常见，而在几乎未捕获到小鼠的采样点中仅检测到1种HIA。ospC等位基因U仅在东部花栗鼠（Tamias striatus）体内被检出；尽管在花栗鼠体内观测到了包括HIAs在内的多种不同等位基因，但等位基因U从未与其他等位基因在混合感染中共存。本研究结果表明，等位基因U可能会排斥其他等位基因，从而削弱花栗鼠作为HIAs储存宿主的能力。