Adaptive immunity in Mus musculus influences the acquisition and abundance of Borrelia burgdorferi in Ixodes scapularis ticks.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Applied and Environmental Microbiology Pub Date : 2024-11-06 DOI:10.1128/aem.01299-24
Cody W Koloski, Hesham Adam, Georgia Hurry, Alexandra Foley-Eby, Christopher B Zinck, Haomiao Wei, Satyender Hansra, Jenny Wachter, Maarten J Voordouw
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Abstract

The Lyme disease spirochete Borrelia burgdorferi cycles between immature black-legged ticks (Ixodes scapularis) and vertebrate reservoir hosts, such as rodents. Larval ticks acquire spirochetes from infected hosts, and the resultant nymphs transmit the spirochetes to naïve hosts. This study investigated the impact of immunocompetence and host tissue spirochete load on host-to-tick transmission (HTT) of B. burgdorferi and the spirochete load inside immature I. scapularis ticks. Wild-type (WT) C57BL/6J mice and mice with severe combined immunodeficiency (SCID) were experimentally infected with B. burgdorferi. To measure HTT, WT and SCID mice were repeatedly infested with I. scapularis larvae, and ticks were sacrificed at three different developmental stages: engorged larvae, 1-month-old, and 12-month-old nymphs. The spirochete loads in immature ticks and mouse tissues were estimated using qPCR. In WT mice, HTT decreased from 90% to 65% over the course of the infection, whereas in the SCID mice, HTT was always 100%. Larvae that fed on SCID mice acquired a much larger dose of spirochetes compared to larvae that fed on WT mice. This difference in spirochete load persisted over tick development where nymphs that fed as larvae on SCID mice had significantly higher spirochete loads compared to their WT counterparts. HTT and the tick spirochete loads were strongly correlated with the mouse tissue spirochete loads. Our study shows that the host immune system (e.g., the presence of antibodies) influences HTT of B. burgdorferi and the spirochete load in immature I. scapularis ticks.IMPORTANCEThe tick-borne spirochete Borrelia burgdorferi causes Lyme disease in humans. This pathogen is maintained in nature by cycles involving black-legged ticks and wildlife hosts. The present study investigated the host factors that influence the transmission of B. burgdorferi from infected hosts to feeding ticks. We infected immunocompetent mice and immunocompromised mice (that cannot develop antibodies) with B. burgdorferi and repeatedly infested these mice with ticks. We determined the percentage of infected ticks and their spirochete loads. This percentage was 100% for immunocompromised mice but decreased from 90% to 65% over time (8 weeks) for immunocompetent mice. The tick spirochete load was much higher in ticks fed on immunocompromised mice compared to ticks fed on immunocompetent mice. In summary, the host immune system influences the transmission of B. burgdorferi from infected hosts to ticks and the spirochete loads in those ticks, which, in turn, determines the risk of Lyme disease for people.

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麝的适应性免疫影响蜱虫中鲍曼不动杆菌的获得和数量。
莱姆病螺旋体包柔氏菌(Borrelia burgdorferi)在未成熟黑腿蜱(Ixodes scapularis)和啮齿动物等脊椎动物宿主之间循环。幼蜱从受感染的宿主身上获得螺旋体,然后由若虫将螺旋体传播给未受感染的宿主。本研究调查了免疫能力和宿主组织螺旋体数量对B. burgdorferi宿主到蜱传播(HTT)以及未成熟蚤蜱体内螺旋体数量的影响。野生型(WT)C57BL/6J小鼠和严重联合免疫缺陷(SCID)小鼠实验性感染了布氏杆菌。为了测量 HTT,用 I. scapularis 幼虫反复侵染 WT 和 SCID 小鼠,并在三个不同的发育阶段(噬血幼虫、1 个月大的幼虫和 12 个月大的若虫)牺牲蜱虫。利用 qPCR 对未成熟蜱和小鼠组织中的螺旋体数量进行了估计。在 WT 小鼠中,HTT 在感染过程中从 90% 降至 65%,而在 SCID 小鼠中,HTT 始终为 100%。与喂养 WT 小鼠的幼虫相比,喂养 SCID 小鼠的幼虫获得的螺旋体剂量要大得多。这种螺旋体数量上的差异在蜱的发育过程中持续存在,以 SCID 小鼠为幼虫喂养的若虫的螺旋体数量明显高于 WT 小鼠。HTT和蜱螺旋体数量与小鼠组织螺旋体数量密切相关。我们的研究表明,宿主的免疫系统(如抗体的存在)会影响HTT的B.burgdorferi和未成熟I.scapularis蜱的螺旋体数量。重要意义蜱传螺旋体鲍瑞氏菌(Borrelia burgdorferi)会导致人类患上莱姆病。这种病原体在自然界中通过黑腿蜱和野生动物宿主的循环来维持。本研究调查了影响包柔氏螺旋体从受感染宿主向摄食蜱传播的宿主因素。我们用布氏杆菌感染免疫功能正常的小鼠和免疫功能低下的小鼠(不能产生抗体),并用蜱虫反复叮咬这些小鼠。我们测定了受感染蜱虫的百分比及其螺旋体数量。免疫力低下的小鼠的感染率为 100%,而免疫力正常的小鼠的感染率则随着时间的推移(8 周)从 90% 降至 65%。与免疫功能正常的小鼠相比,喂养免疫功能低下小鼠的蜱的螺旋体数量要高得多。总之,宿主免疫系统会影响布氏杆菌从受感染宿主向蜱虫的传播以及蜱虫体内的螺旋体数量,进而决定人类患莱姆病的风险。
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来源期刊
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
期刊最新文献
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