CRBM, University of Montpellier, CNRS, Montpellier, France.
Laboratoire de Génétique et Pathologie des Mollusques Marins, Ifremer, La Tremblade, France.
PLoS Negl Trop Dis. 2021 Jan 6;15(1):e0008935. doi: 10.1371/journal.pntd.0008935. eCollection 2021 Jan.
Brugia malayi is a human filarial nematode responsible for elephantiasis, a debilitating condition that is part of a broader spectrum of diseases called filariasis, including lymphatic filariasis and river blindness. Almost all filarial nematode species infecting humans live in mutualism with Wolbachia endosymbionts, present in somatic hypodermal tissues but also in the female germline which ensures their vertical transmission to the nematode progeny. These α-proteobacteria potentially provision their host with essential metabolites and protect the parasite against the vertebrate immune response. In the absence of Wolbachia wBm, B. malayi females become sterile, and the filarial nematode lifespan is greatly reduced. In order to better comprehend this symbiosis, we investigated the adaptation of wBm to the host nematode soma and germline, and we characterized these cellular environments to highlight their specificities. Dual RNAseq experiments were performed at the tissue-specific and ovarian developmental stage levels, reaching the resolution of the germline mitotic proliferation and meiotic differentiation stages. We found that most wBm genes, including putative effectors, are not differentially regulated between infected tissues. However, two wBm genes involved in stress responses are upregulated in the hypodermal chords compared to the germline, indicating that this somatic tissue represents a harsh environment to which wBm have adapted. A comparison of the B. malayi and C. elegans germline transcriptomes reveals a poor conservation of genes involved in the production of oocytes, with the filarial germline proliferative zone relying on a majority of genes absent from C. elegans. The first orthology map of the B. malayi genome presented here, together with tissue-specific expression enrichment analyses, indicate that the early steps of oogenesis are a developmental process involving genes specific to filarial nematodes, that likely result from evolutionary innovations supporting the filarial parasitic lifestyle.
班氏吴策线虫是一种引起象皮病的人类丝虫，这是一种使人虚弱的疾病，属于更广泛的丝虫病范畴，包括淋巴丝虫病和河盲症。几乎所有感染人类的丝虫都与沃尔巴克氏体共生，这种共生体存在于体皮下组织中，也存在于雌性生殖系中，这确保了它们垂直传递给丝虫后代。这些α-变形菌可能为宿主提供必需的代谢物，并保护寄生虫免受脊椎动物免疫反应的影响。在没有沃尔巴克氏体 wBm 的情况下，班氏吴策线虫的雌性会变得不育，并且丝虫的寿命大大缩短。为了更好地理解这种共生关系，我们研究了 wBm 对宿主线虫体和生殖系的适应，并对这些细胞环境进行了特征描述，以突出它们的特异性。我们在组织特异性和卵巢发育阶段水平上进行了双 RNAseq 实验，达到了生殖系有丝分裂增殖和减数分裂分化阶段的分辨率。我们发现，大多数 wBm 基因，包括假定的效应子，在感染组织中没有差异表达。然而，两个参与应激反应的 wBm 基因在体壁索中相对于生殖系上调，这表明这种体壁组织是 wBm 适应的恶劣环境。班氏吴策线虫和秀丽隐杆线虫生殖系转录组的比较显示，参与卵母细胞产生的基因保守性较差，而丝虫生殖系增殖区依赖于大多数秀丽隐杆线虫所没有的基因。这里提出的班氏吴策线虫基因组的第一个同源图谱，以及组织特异性表达富集分析，表明卵母细胞发生的早期步骤是一个涉及丝虫特异性基因的发育过程，这可能是支持丝虫寄生生活方式的进化创新的结果。
