A novel tick protein supports integrity of gut peritrophic matrix impacting existence of gut microbiome and Lyme disease pathogens,Cellular Microbiology

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A novel tick protein supports integrity of gut peritrophic matrix impacting existence of gut microbiome and Lyme disease pathogens
Cellular Microbiology ( IF 2.6 ) Pub Date : 2020-10-01 , DOI: 10.1111/cmi.13275
Xiuli Yang ₁ , Juraj Koči _{2,

3} , Alexis A Smith ₁ , Xuran Zhuang ₁ , Kavita Sharma ₁ , Shraboni Dutta ₁ , Vipin S Rana ₁ , Chrysoula Kitsou ₁ , Ozlem B Yas ₄ , Emmanuel F Mongodin ₅ , Utpal Pal _{1,

6}

Affiliation

The peritrophic matrix (PM) is an acellular membrane that covers the gut epithelium in arthropods and physically separates it from the lumen. The structure is thought to play an important role in tick biology. The PM is also known to impact the persistence of tick‐borne pathogens like Borrelia burgdorferi, although limited information is available about its molecular constituents or their biological significance. Herein, we characterise a novel PM‐associated gut protein in Ixodes scapularis ticks, annotated as Peritrophic Membrane Chitin Binding Protein (PM_CBP), for its role in the integrity and function of the matrix. The PM_CBP displays homology to the chitin deacetylase metalloenzyme, shows upregulation during tick feeding, and is localized at the luminal surface of the gut epithelium. The structural integrity of the PM was impaired both by the knock down of PM_CBP expression via RNA interference and by treatment with anti‐PM_CBP antibodies, as revealed by its electron microscopic appearance. Additionally, the duration of tick engorgement on mice and the passage of experimentally‐inoculated fluorescent dextran molecules across the PM are affected by the knock down of PM_CBP expression. The transfer of anti‐PM_CBP antibodies into the tick gut impacted the overall composition of the resident microbiome, and also influenced B. burgdorferi acquisition in ticks and its transmission to mice. Taken together, these data highlight the biological significance of the Ixodes PM and suggest that the targeting of its molecular constituents may contribute to the development of novel interventions against tick‐borne infections.

中文翻译：

一种新的蜱蛋白支持肠道营养基质的完整性，影响肠道微生物组和莱姆病病原体的存在

peritrophic matrix (PM) 是一种无细胞膜，覆盖节肢动物的肠上皮，并将其与管腔物理隔开。该结构被认为在蜱生物学中起重要作用。众所周知，PM 会影响蜱传病原体（如伯氏疏螺旋体）的持久性，尽管关于其分子成分或其生物学意义的信息有限。在这里，我们描述了肩胛硬蜱蜱中一种新的 PM 相关肠道蛋白，注释为P eritrophic M embrane C hitin B inding P蛋白（PM_CBP），因其在矩阵的完整性和功能中的作用。PM_CBP 与几丁质去乙酰化酶金属酶具有同源性，在蜱喂养期间显示上调，并且位于肠上皮的腔表面。PM 的结构完整性受到RNA 干扰抑制PM_CBP表达和抗 PM_CBP 抗体处理的损害，如其电子显微镜外观所示。此外，小鼠蜱充血的持续时间和实验接种的荧光葡聚糖分子通过 PM 受到PM_CBP表达的抑制。抗 PM_CBP 抗体转移到蜱肠道影响了常驻微生物组的整体组成，也影响了B. burgdorferi在蜱中的获得及其对小鼠的传播。总之，这些数据突出了硬蜱PM 的生物学意义，并表明靶向其分子成分可能有助于开发针对蜱传感染的新型干预措施。

更新日期：2020-10-01

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