Abstract

BackgroundLateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in ~20% of arthropod and nematode genome sequencing projects. Many of these transfers are large and contain a substantial part of the Wolbachia genome.ResultsHere, we re-sequenced three D. ananassae genomes from Asia and the Pacific that contain large LGTs from Wolbachia. We find that multiple copies of the Wolbachia genome are transferred to the Drosophila nuclear genome in all three lines. In the D. ananassae line from Indonesia, the copies of Wolbachia DNA in the nuclear genome are nearly identical in size and sequence yielding an even coverage of mapped reads over the Wolbachia genome. In contrast, the D. ananassae lines from Hawaii and India show an uneven coverage of mapped reads over the Wolbachia genome suggesting that different parts of these LGTs are present in different copy numbers. In the Hawaii line, we find that this LGT is underrepresented in third instar larvae indicative of being heterochromatic. Fluorescence in situ hybridization of mitotic chromosomes confirms that the LGT in the Hawaii line is heterochromatic and represents ~20% of the sequence on chromosome 4 (dot chromosome, Muller element F).ConclusionsThis collection of related lines contain large lateral gene transfers composed of multiple Wolbachia genomes that constitute >2% of the D. ananassae genome (~5 Mbp) and partially explain the abnormally large size of chromosome 4 in D. ananassae.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1097) contains supplementary material, which is available to authorized users.

Highlights

  • Lateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in ~20% of arthropod and nematode genome sequencing projects

  • Because sequence data from contaminating Wolbachia bacteria would complicate the analysis of the nuwt, the flies were treated with tetracycline for three generations prior to DNA extraction in order to create Wbnuwt+ lines

  • To further ensure the absence of Wolbachia DNA originating from the bacterial genome rather than the nuwt in the sequencing data, the ovaries of tet-treated flies were confirmed to be Wb- by fluorescence in situ hybridization (FISH) microscopy with Wolbachia-infected flies serving as a positive control

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Summary

Introduction

Lateral gene transfer (LGT) from bacterial Wolbachia endosymbionts has been detected in ~20% of arthropod and nematode genome sequencing projects. Many of these transfers are large and contain a substantial part of the Wolbachia genome. Lateral gene transfer (LGT) can be defined as the transfer of DNA between organisms that does not result from sexual reproduction. Wolbachia endosymbionts are bacteria that colonize filarial nematodes and several different arthropods, including >20% of insect species [2,3,4]. While obligate mutualists in nematodes, Wolbachia are best known for the ability to manipulate host reproduction in arthropods in various ways which include induction of parthenogenesis, feminization, male killing, and cytoplasmic incompatibility [2]. As some strains have been shown to target the germline stem cell niche [5], these endosymbionts are ideally located to bring about heritable LGT to eukaryotic genomes [6,7], since they colonize the cells that will give rise to the germ line and offspring

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