Function and evolution of the aquaporin IsAQP1 in the Lyme disease vector Ixodes scapularis

Function and evolution of the aquaporin IsAQP1 in the Lyme disease vector Ixodes scapularis
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DOI:
10.1111/imb.12833
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发表时间:
2023-02-22
影响因子:
2.6
通讯作者:
Rasgon,Jason L. L.
Rasgon,Jason L. L.
中科院分区:
农林科学2区
文献类型:
--
作者:
Tsujimoto,Hitoshi;Metz,Hillery C. C.;Rasgon,Jason L. L.

文献摘要

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蜱是人类、野生动物和家畜致病病毒、细菌和原生动物的重要载体。由于它们的生命周期,蜱面临着与水稳态相关的重大挑战。当吸血时,它们必须排出水和离子,但当离开宿主(持续数月)时,它们必须保存水分以避免干燥。水通道蛋白(AQP)是一种膜结合水通道家族,是许多动物中调节呼吸的关键因素,但在蜱中的特征仍然很差。在这里,我们从鹿蜱肩胛硬蜱中生物信息学鉴定了AQP样基因,并使用系统发育方法绘制了节肢动物水通道蛋白基因家族的进化图。大多数蛛形纲动物的AQP样序列(包括肩胛硬蜱)形成了一个单系群,聚集在从细菌到脊椎动物的水甘油孔蛋白(GLP)中。该基因家族在昆虫中不存在,揭示了不同吸血节肢动物中AQP的不同进化路径。接下来,我们测序了肩胛骨I. scapulatum aquaporin 1(IsAQP1)的全长cDNA,并在异种卵母细胞中异源表达,以功能性地表征其对水和溶质的渗透性。此外,我们还研究了IsAQP 1在不同生命阶段和成年女性器官中的表达。我们发现IsAQP1是一个高效的水通道,在摄食前的唾液腺中高表达,提示其在摄食前或摄食过程中起着重要的调节作用。它的功能特性是独特的:与大多数GLP不同,IsAQP 1具有低甘油渗透性,与大多数AQP不同,它对汞不敏感。总之,我们的研究结果表明,AQP1在蜱水平衡生理学中起着重要作用,它可能有望成为新型载体控制工作的目标。
Ticks are important vectors of pathogenic viruses, bacteria, and protozoans to humans, wildlife, and domestic animals. Due to their life cycles, ticks face significant challenges related to water homeostasis. When blood‐feeding, they must excrete water and ions, but when off‐host (for stretches lasting several months), they must conserve water to avoid desiccation. Aquaporins (AQPs), a family of membrane‐bound water channels, are key players in osmoregulation in many animals but remain poorly characterized in ticks. Here, we bioinformatically identified AQP‐like genes from the deer tickIxodes scapularisand used phylogenetic approaches to map the evolution of the aquaporin gene family in arthropods. Most arachnid AQP‐like sequences (including those ofI. scapularis) formed a monophyletic group clustered within aquaglycerolporins (GLPs) from bacteria to vertebrates. This gene family is absent from insects, revealing divergent evolutionary paths for AQPs in different hematophagous arthropods. Next, we sequenced the full‐length cDNA ofI. scapularisaquaporin 1 (IsAQP1) and expressed it heterologously inXenopusoocytes to functionally characterize its permeability to water and solutes. Additionally, we examinedIsAQP1expression across different life stages and adult female organs. We foundIsAQP1is an efficient water channel with high expression in salivary glands prior to feeding, suggesting it plays a role in osmoregulation before or during blood feeding. Its functional properties are unique: unlike most GLPs,IsAQP1has low glycerol permeability, and unlike most AQPs, it is insensitive to mercury. Together, our results suggestIsAQP1plays an important role in tick water balance physiology and that it may hold promise as a target of novel vector control efforts.