Transcriptomic responses of Biomphalaria pfeifferi to Schistosoma mansoni: Investigation of a neglected African snail that supports more S. mansoni transmission than any other snail species,PLOS Neglected Tropical Diseases

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Transcriptomic responses of Biomphalaria pfeifferi to Schistosoma mansoni: Investigation of a neglected African snail that supports more S. mansoni transmission than any other snail species
PLOS Neglected Tropical Diseases ( IF 3.4 ) Pub Date : 2017-10-18 , DOI: 10.1371/journal.pntd.0005984
Sarah K Buddenborg ₁ , Lijing Bu ₁ , Si-Ming Zhang ₁ , Faye D Schilkey ₂ , Gerald M Mkoji ₃ , Eric S Loker ₁

Affiliation

Background

Biomphalaria pfeifferi is highly compatible with the widespread human-infecting blood fluke Schistosoma mansoni and transmits more cases of this parasite to people than any other snail species. For these reasons, B. pfeifferi is the world’s most important vector snail for S. mansoni, yet we know relatively little at the molecular level regarding the interactions between B. pfeifferi and S. mansoni from early-stage sporocyst transformation to the development of cercariae.

Methodology/Principal findings

We sought to capture a portrait of the response of B. pfeifferi to S. mansoni as it occurs in nature by undertaking Illumina dual RNA-Seq on uninfected control B. pfeifferi and three intramolluscan developmental stages (1- and 3-days post infection and patent, cercariae-producing infections) using field-derived west Kenyan specimens. A high-quality, well-annotated de novo B. pfeifferi transcriptome was assembled from over a half billion non-S. mansoni paired-end reads. Reads associated with potential symbionts were noted. Some infected snails yielded fewer normalized S. mansoni reads and showed different patterns of transcriptional response than others, an indication that the ability of field-derived snails to support and respond to infection is variable. Alterations in transcripts associated with reproduction were noted, including for the oviposition-related hormone ovipostatin and enzymes involved in metabolism of bioactive amines like dopamine or serotonin. Shedding snails exhibited responses consistent with the need for tissue repair. Both generalized stress and immune factors immune factors (VIgLs, PGRPs, BGBPs, complement C1q-like, chitinases) exhibited complex transcriptional responses in this compatible host-parasite system.

Significance

This study provides for the first time a large sequence data set to help in interpreting the important vector role of the neglected snail B. pfeifferi in transmission of S. mansoni, including with an emphasis on more natural, field-derived specimens. We have identified B. pfeifferi targets particularly responsive during infection that enable further dissection of the functional role of these candidate molecules.

中文翻译：

Biomphalaria pfeifferi 对曼氏血吸虫的转录组反应：对一种被忽视的非洲蜗牛的调查，该蜗牛比任何其他蜗牛物种支持更多的曼氏血吸虫传播

背景

菲氏双脐螺与广泛传播的人类感染血吸虫曼氏血吸虫高度相容，并且将这种寄生虫传播给人类的病例比任何其他蜗牛物种都多。由于这些原因， B . pfeifferi是世界上最重要的媒介蜗牛。 mansoni ，但我们在分子水平上对B之间的相互作用知之甚少。菲佛里和 S .曼索尼从早期孢子囊转化到尾蚴的发育。

方法/主要发现

我们试图描绘B的反应。菲佛里到S .通过对未感染的对照B进行 Illumina 双 RNA-Seq 来检测自然界中存在的曼氏菌。使用来自西肯尼亚的野外标本，研究了pfeifferi和三个软体动物内发育阶段（感染后 1 天和 3 天以及明显的、产生尾蚴的感染）。 A 高质量、注释完善的de novo B . pfeifferi转录组由超过5亿个非S. pfeifferi转录组组装而成。曼索尼双端读。注意到与潜在共生体相关的读取。一些受感染的蜗牛产生较少的标准化S 。曼索尼读取并显示出与其他蜗牛不同的转录反应模式，这表明田间蜗牛支持和应对感染的能力是可变的。注意到与繁殖相关的转录本的改变，包括与产卵相关的激素卵抑素和参与生物活性胺（如多巴胺或血清素）代谢的酶。脱落的蜗牛表现出与组织修复需求一致的反应。广义应激和免疫因子（VIgL、PGRP、BGBP、补体 C1q 样、几丁质酶）在这种兼容的宿主-寄生虫系统中表现出复杂的转录反应。