Parasites modulate the gut-microbiome in insects: A proof-of-concept study

Parasites modulate the gut-microbiome in insects: A proof-of-concept study
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DOI:
10.1371/journal.pone.0227561
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发表时间:
2020-01-14
期刊:
影响因子:
3.7
通讯作者:
Kapel, Christian M. O.
Kapel, Christian M. O.
中科院分区:
综合性期刊3区
文献类型:
--
作者:
Fredensborg, Brian L.;Fossdal i Kalvalio, Inga;Kapel, Christian M. O.

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宿主与寄生虫的相互作用可能受到宿主或寄生虫相关微生物的调节,但它们的作用往往被忽视。特别是对于具有肠道阶段的寄生虫(无论是幼虫还是成虫),宿主肠道微生物群可能对寄生虫的建立起关键作用;此外,微生物组可能会对入侵的寄生虫做出反应。由于伦理、后勤和经济方面的限制,在生物体水平上的假设检验可能受到阻碍,特别是在哺乳动物最终宿主中。因此,无脊椎动物作为具有复杂生命周期的寄生虫的中间宿主,可能为哺乳动物模型的早期宿主-寄生虫模型的发展提供了信息。此外,一些重要的病原体是由昆虫传播的,昆虫肠道微生物群与病原体的相互作用可能提供必要的基线知识,可用于控制媒介传播的病原体。在这里,我们使用谷物甲虫,小膜绦虫的宿主,在感染后的两个预先确定的时间点(第2天和第7天)探索感染状态和常驻肠道微生物群之间的相互作用。利用16S/18S微生物谱,我们测量了宿主肠道细菌组和真菌组的组成、相对丰度和多样性的关键参数。此外,我们通过酚氧化酶活性和血细胞丰度量化了甲虫对感染的全身免疫反应。我们发现肠道细菌组和真菌组的显著变化与感染状态和甲虫年龄有关。因此,受感染的甲虫肠道中变形杆菌的相对丰度明显较高,主要是由不动杆菌的丰度增加引起的。此外,与未感染的甲虫相比,感染甲虫的真菌群落数量较少,但Shannon多样性较高。与未处理的对照组相比,使用广谱抗生素(四环素)处理的甲虫显示出明显减少的寄生虫建立,这表明宿主微生物组可能极大地影响了H. diminuta幼虫的孵化和随后的建立。我们的研究结果表明,使用无脊椎动物的实验工作可能为宿主-寄生虫-微生物相互作用及其潜在机制的探索性研究提供了一个平台。
Host-parasite interactions may be modulated by host- or parasite-associated microbes, but the role of these are often overlooked. Particularly for parasites with intestinal stages (either larval or adult), the host gut microbiome may play a key role for parasite establishment; moreover, the microbiome may change in response to invading parasites. Hypothesis testing at the organismal level may be hampered, particularly in mammalian definitive hosts, by ethical, logistical, and economical restrictions. Thus, invertebrates naturally serving as intermediate hosts to parasites with complex life cycles may inform the development of mammalian models as an early-stage host-parasite model. In addition, several important pathogens are vectored by insects, and insect gut microbiome-pathogen interactions may provide essential base-line knowledge, which may be used to control vectorborne pathogens. Here, we used the grain beetle, Tenebrio molitor, a host of the tapeworm Hymenolepis diminuta, to explore interactions between infection status and resident gut microbiota at two pre-determined time points (day two and seven) post infection. Using 16S/18S microbial profiling, we measured key parameters of the composition, relative abundance, and diversity of the host gut bacteriome and mycobiome. In addition, we quantified the systemic beetle immune response to infection by Phenoloxidase activity and hemocyte abundance. We found significant changes in the gut bacteriome and mycobiome in relation to infection status and beetle age. Thus, the relative abundance of Proteobacteria was significantly higher in the gut of infected beetles and driven mostly by an increased abundance of Acinetobacter. In addition, the mycobiome was less abundant in infected beetles but maintained higher Shannon diversity in infected compared with non-infected beetles. Beetles treated with a broad-spectrum antibiotic (Tetracycline) exhibited significantly reduced parasite establishment compared with the untreated control group, indicating that the host microbiome may greatly influence hatching of eggs and subsequent establishment of H. diminuta larvae. Our results suggest that experimental work using invertebrates may provide a platform for explorative studies of host-parasite-microbe interactions and their underlying mechanisms.