Dual RNAseq analyses at soma and germline levels reveal evolutionary innovations in the elephantiasis-agent Brugia malayi, and adaptation of its Wolbachia endosymbionts

Type Article
Date 2021-01
Language English
Author(s) Chevignon GermainORCID1, 2, Foray VincentORCID1, 3, Pérez-Jiménez Mercedes MariaORCID1, 4, Libro Silvia5, Chung MatthewORCID6, Foster Jeremy M.ORCID5, Landmann FrédéricORCID1
Affiliation(s) 1 : CRBM, University of Montpellier, CNRS, Montpellier, France
2 : Laboratoire de Génétique et Pathologie des Mollusques Marins, Ifremer, La Tremblade, France
3 : Institut de Recherche sur la Biologie de l’Insecte, UMR 7261, CNRS, Université de Tours, Tours, France
4 : Centro Andaluz de Biología del Desarrollo (CABD)–Universidad Pablo de Olavide (UPO), Departamento de Biología Molecular e Ingeniería Bioquímica, UPO/CSIC/JA, Sevilla, Spain
5 : Division of Protein Expression & Modification, New England Biolabs, Ipswich, Massachusetts, United States of America
6 : Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America, Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America
Source Plos Neglected Tropical Diseases (1935-2735) (Public Library of Science (PLoS)), 2021-01 , Vol. 15 , N. 1 , P. e0008935 (26p.)
DOI 10.1371/journal.pntd.0008935
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.

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Publisher's official version 26 3 MB Open access
S1 Fig. Validation of differential gene expressions in PZ, MZ and BW RNAseq analyses cDNAs were produced using total RNA extracted from pools of 60 PZ, 60 MZ and 30 BW fragments for each of ... 8 MB Open access
S1 Table. wBm gene expression data in PZ, MZ and BW, compared between samples as follows: PZ vs MZ; PZ vs BW; MZ vs BW. 1 MB Open access
S2 Table. B. malayi gene expression data in PZ, MZ and BW, compared between samples as follows: PZ vs MZ; PZ vs BW; MZ vs BW. 15 MB Open access
S3 Table. B. malayi expression data of genes specifically up regulated in PZ and MZ. 1 MB Open access
S4 Table. List of genes without Wormbase ID or not present in the Compara database. 46 KB Open access
S5 Table. List of primers used in RT-PCR and qRT-PCR to confirm selected gene expression levels of RNAseq data. 10 KB Open access
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How to cite 

Chevignon Germain, Foray Vincent, Pérez-Jiménez Mercedes Maria, Libro Silvia, Chung Matthew, Foster Jeremy M., Landmann Frédéric (2021). Dual RNAseq analyses at soma and germline levels reveal evolutionary innovations in the elephantiasis-agent Brugia malayi, and adaptation of its Wolbachia endosymbionts. Plos Neglected Tropical Diseases, 15(1), e0008935 (26p.). Publisher's official version : https://doi.org/10.1371/journal.pntd.0008935 , Open Access version : https://archimer.ifremer.fr/doc/00668/77991/