Abstract
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.
Highlights
With an estimated excess of a million species, the phylum Nematoda alone constitutes ~80% of the multicellular organisms on earth, with its members having colonized all regions of the world [1]
Almost all species infecting humans live in mutualism with Wolbachia endosymbionts
The Wolbachia wBm of Brugia malayi, a nematode responsible for human elephantiasis, show a typical localisation in the hypodermis of the adult worms, and in the female germline in order to be vertically transmitted to the generation through the eggs
Summary
With an estimated excess of a million species, the phylum Nematoda alone constitutes ~80% of the multicellular organisms on earth, with its members having colonized all regions of the world [1]. Clade III harbors parasitic species engaged in mutualistic symbiosis. It encompasses the family Onchocercidae, called filariae or filarial nematodes. Their third larval stage is infective and transmitted by haematophagous arthropods to vertebrate hosts, in which adult filarial worms reproduce predominantly in the lymphatics, subcutaneously, or in the serous cavity [5]. About 40% of all filarial species live in association with Wolbachia endosymbionts [6], a genus of intracellular obligate alpha-proteobacteria widely present among arthropods, but limited to the Onchocercidae family in animal parasitic nematodes [7]. The Wolbachia represent a monophyletic bacterial genus sub-divided into supergroups, with some specific to filarial nematodes [7,8]. Each Wolbachia strain has its genomic specificities, and phylogenetic studies have revealed a strong co-evolution between Wolbachia and their filarial host species [6]
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