Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi.

Panagiotis Ioannidis,James R White,Nikhil Kumar,Karen T Olarte,Mark J Taylor,Kelly L Johnston,Sandra Ott,David R Riley,Jeremy M Foster,Julie C Dunning Hotopp,Luke J Tallon

doi:10.1186/1471-2164-14-639

Abstract

BackgroundLymphatic filariasis is a neglected tropical disease afflicting more than 120 million people, while another 1.3 billion people are at risk of infection. The nematode worm Brugia malayi is one of the causative agents of the disease and exists in a mutualistic symbiosis with Wolbachia bacteria. Since extensive lateral gene transfer occurs frequently between Wolbachia and its hosts, we sought to measure the extent of such LGT in B. malayi by whole genome sequencing of Wolbachia-depleted worms.ResultsA considerable fraction (at least 115.4-kbp, or 10.6%) of the 1.08-Mbp Wolbachia wBm genome has been transferred to its nematode host and retains high levels of similarity, including 227 wBm genes and gene fragments. Complete open reading frames were transferred for 32 of these genes, meaning they have the potential to produce functional proteins. Moreover, four transfers have evidence of life stage-specific regulation of transcription at levels similar to other nematode transcripts, strengthening the possibility that they are functional.ConclusionsThere is extensive and ongoing transfer of Wolbachia DNA to the worm genome and some transfers are transcribed in a stage-specific manner at biologically relevant levels.

Highlights

Lymphatic filariasis is a neglected tropical disease afflicting more than 120 million people, while another 1.3 billion people are at risk of infection
Wolbachia depletion of Brugia malayi worms and DNA sequencing Since B. malayi has a mutualistic symbiotic relationship with Wolbachia strain wBm, such that neither symbiotic partner can survive without the other, the B. malayi genome cannot be sequenced without sequencing the Wolbachia genome
Worms used for sequencing were treated with tetracycline to deplete the Wolbachia endosymbionts

Summary

Introduction

Lymphatic filariasis is a neglected tropical disease afflicting more than 120 million people, while another 1.3 billion people are at risk of infection. Since extensive lateral gene transfer occurs frequently between Wolbachia and its hosts, we sought to measure the extent of such LGT in B. malayi by whole genome sequencing of Wolbachia-depleted worms. Brugia malayi (filarial nematode) is a causative agent of human lymphatic filariasis, a neglected tropical disease that results in elephantiasis and disability, handicap, and stigma. Efforts at combating the disease include mass drug administration to reduce the blood levels of During the original whole genome sequencing of B. malayi extensive levels of lateral gene transfer (LGT) were identified from its Wolbachia endosymbiont, wBm [4]. Such LGTs are called nuwts for nuclear Wolbachia transfers following the established nomenclature for numts for nuclear mitochondrial DNA segments

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