Defining Brugia malayi and Wolbachia symbiosis by stage-specific dual RNA-seq

Alexandra Grote, Denis Voronin, Tao Ding, Alan Twaddle, Thomas R. Unnasch, Sara Lustigman, Elodie Ghedin

Research output: Contribution to journalArticle

Abstract

Background: Filarial nematodes currently infect up to 54 million people worldwide, with millions more at risk for infection, representing the leading cause of disability in the developing world. Brugia malayi is one of the causative agents of lymphatic filariasis and remains the only human filarial parasite that can be maintained in small laboratory animals. Many filarial nematode species, including B. malayi, carry an obligate endosymbiont, the alpha-proteobacteria Wolbachia, which can be eliminated through antibiotic treatment. Elimination of the endosymbiont interferes with development, reproduction, and survival of the worms within the mamalian host, a clear indicator that the Wolbachia are crucial for survival of the parasite. Little is understood about the mechanism underlying this symbiosis. Methodology/ Principle findings: To better understand the molecular interplay between these two organisms we profiled the transcriptomes of B. malayi and Wolbachia by dual RNA-seq across the life cycle of the parasite. This helped identify functional pathways involved in this essential symbiotic relationship provided by the co-expression of nematode and bacterial genes. We have identified significant stage-specific and gender-specific differential expression in Wolbachia during the nematode’s development. For example, during female worm development we find that Wolbachia upregulate genes involved in ATP production and purine biosynthesis, as well as genes involved in the oxidative stress response. Conclusions/ Significance: This global transcriptional analysis has highlighted specific pathways to which both Wolbachia and B. malayi contribute concurrently over the life cycle of the parasite, paving the way for the development of novel intervention strategies.

Original languageEnglish (US)
Article numbere0005357
JournalPLoS Neglected Tropical Diseases
Volume11
Issue number3
DOIs
StatePublished - Mar 30 2017

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Brugia malayi
Wolbachia
Symbiosis
RNA
Parasites
Life Cycle Stages
Filarial Elephantiasis
Alphaproteobacteria
Bacterial Genes
Laboratory Animals
Transcriptome
Genes
Reproduction
Oxidative Stress
Up-Regulation
Adenosine Triphosphate
Anti-Bacterial Agents
Survival
Infection

ASJC Scopus subject areas

  • Pharmacology, Toxicology and Pharmaceutics(all)
  • Public Health, Environmental and Occupational Health
  • Infectious Diseases

Cite this

Defining Brugia malayi and Wolbachia symbiosis by stage-specific dual RNA-seq. / Grote, Alexandra; Voronin, Denis; Ding, Tao; Twaddle, Alan; Unnasch, Thomas R.; Lustigman, Sara; Ghedin, Elodie.

In: PLoS Neglected Tropical Diseases, Vol. 11, No. 3, e0005357, 30.03.2017.

Research output: Contribution to journalArticle

Grote A, Voronin D, Ding T, Twaddle A, Unnasch TR, Lustigman S et al. Defining Brugia malayi and Wolbachia symbiosis by stage-specific dual RNA-seq. PLoS Neglected Tropical Diseases. 2017 Mar 30;11(3). e0005357. https://doi.org/10.1371/journal.pntd.0005357
Grote, Alexandra ; Voronin, Denis ; Ding, Tao ; Twaddle, Alan ; Unnasch, Thomas R. ; Lustigman, Sara ; Ghedin, Elodie. / Defining Brugia malayi and Wolbachia symbiosis by stage-specific dual RNA-seq. In: PLoS Neglected Tropical Diseases. 2017 ; Vol. 11, No. 3.
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