Nimbus (BgI): An active non-LTR retrotransposon of the Schistosoma mansoni snail host Biomphalaria glabrata

Biomedical Research Institute (BRI), 12111 Parklawn Drive, Rockville, MD 20852, USA.
International Journal for Parasitology (Impact Factor: 3.87). 11/2007; 37(12):1307-18. DOI: 10.1016/j.ijpara.2007.04.002
Source: PubMed


The freshwater snail Biomphalaria glabrata is closely associated with the transmission of human schistosomiasis. An ecologically sound method has been proposed to control schistosomiasis using genetically modified snails to displace endemic, susceptible ones. To assess the viability of this form of biological control, studies towards understanding the molecular makeup of the snail relative to the presence of endogenous mobile genetic elements are being undertaken since they can be exploited for genetic transformation studies. We previously cloned a 1.95kb BamHI fragment in B. glabrata (BGR2) with sequence similarity to the human long interspersed nuclear element (LINE or L1). A contiguous, full-length sequence corresponding to BGR2, hereafter-named nimbus (BgI), has been identified from a B. glabrata bacterial artificial chromosome (BAC) library. Sequence analysis of the 65,764bp BAC insert contained one full-length, complete nimbus (BgI) element (element I), two full-length elements (elements II and III) containing deletions and flanked by target site duplications and 10 truncated copies. The intact nimbus (BgI) contained two open-reading frames (ORFs 1 and 2) encoding the characteristic hallmark domains found in non-long terminal repeat retrotransposons belonging to the I-clade; a nucleic acid binding protein in ORF1 and an apurinic/apyrimidinic endonuclease, reverse transcriptase and RNase H in ORF2. Phylogenetic analysis revealed that nimbus (BgI) is closely related to Drosophila (I factor), mosquito Aedes aegypti (MosquI) and chordate ascidian Ciona intestinalis (CiI) retrotransposons. Nimbus (BgI) represents the first complete mobile element characterised from a mollusk that appears to be transcriptionally active and is widely distributed in snails of the neotropics and the Old World.

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Available from: Andre Miller
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    • "Normally, the reverse transcriptase domain is the conserved region most commonly found in retroelements and used to construct phylogenetic trees. Phylogenetic analysis of the deduced amino acid sequence of the reverse transcriptase domain of ASDE revealed homology to the I clade of non-LTR retrotransposons including Idt, Idm, BgI, BGR and LSNONLTR1 [2,5,6]. The transcriptionally active BgI element has been reported to be widely distributed in New World and Old World snails [6]. "
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    ABSTRACT: Abdominal segment deformity disease (ASDD) of cultivated whiteleg shrimp Penaeus (Litopenaeus) vannamei causes economic loss of approximately 10% in affected specimens because of the unsightliness of distorted abdominal muscles. It is associated with the presence of viral-like particles seen by electron microscopy in the ventral nerve cords of affected shrimp. Thus, shotgun cloning was carried out to seek viral-like sequences in affected shrimp. A new retrovirus-like element of 5052 bp (named abdominal segment deformity element or ASDE) was compiled by shotgun cloning and 3[prime] and 5[prime] RACE using RNA and DNA extracted from ventral nerve cords of ASDD shrimp. ASDE contained 7 putative open reading frames (ORF). One ORF (called the PENS sub-domain), had a deduced amino acid (aa) sequence homologous to the GIY-YIG endonuclease domain of penelope-like retrotransposons while two others were homologous to the reverse transcriptase (RT) and RNaseH domains of the pol gene of non-long terminal repeat (non-LTR) retrotransposons (called the NLRS sub-domain). No single amplicon of 5 kb containing both these elements was obtained by PCR or RT-PCR from ASDD shrimp. Subsequent analysis indicated that PENS and NLRS were not contiguous and that NLRS was a host genetic element. In situ hybridization using a dioxygenin-labeled NLRS probe revealed that NLRS gave positive reactions in abdominal-ganglion neurons of ASDD shrimp but not normal shrimp. Preliminary analysis indicated that long-term use of female broodstock after eyestalk ablation in the hatchery increased the intensity of RT-PCR amplicons for NLRS and also the prevalence of ASDD in mysis 3 offspring of the broodstock. The deformities persist upon further cultivation until shrimp harvest but do not increase in prevalence and do not affect growth or survival. Our results suggested that NLRS is a shrimp genetic element associated with ASDD and that immediate preventative measures could include shorter-term use of broodstock after eyestalk ablation and/or discard of broodstock that give strong RT-PCR reactions for NLRS. In the longer term, it is recommended, if possible, that currently used, domesticated shrimp lines be selected for freedom from NLRS. The molecular tools developed in this work will facilitate the management and further study of ASDD.
    Full-text · Article · Sep 2013 · BMC Veterinary Research
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    • "The bisulfite sequencing analysis targeted the non LTR-retrotransposon nimbus (BgI) [29], a Mobile Genetic Element (MGE) that is constitutively expressed in naïve B. glabrata and its transcription is enhanced upon stress conditions (heat shock and S. mansoni infection) [30]. An estimated 100 copies of BgI are present in the B. glabrata genome [29]. We detected 22 sites of CpG methylation in a 752 bp region of BgI, and observed variation in the methylation status of the particular CpG sites among the clones that were analysed. "
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    ABSTRACT: Background Biomphalaria glabrata is the mollusc intermediate host for Schistosoma mansoni, a digenean flatworm parasite that causes human intestinal schistosomiasis. An estimated 200 million people in 74 countries suffer from schistosomiasis, in terms of morbidity this is the most severe tropical disease after malaria. Epigenetic information informs on the status of gene activity that is heritable, for which changes are reversible and that is not based on the DNA sequence. Epigenetic mechanisms generate variability that provides a source for potentially heritable phenotypic variation and therefore could be involved in the adaptation to environmental constraint. Phenotypic variations are particularly important in host-parasite interactions in which both selective pressure and rate of evolution are high. In this context, epigenetic changes are expected to be major drivers of phenotypic plasticity and co-adaptation between host and parasite. Consequently, with characterization of the genomes of invertebrates that are parasite vectors or intermediate hosts, it is also essential to understand how the epigenetic machinery functions to better decipher the interplay between host and parasite. Methods The CpGo/e ratios were used as a proxy to investigate the occurrence of CpG methylation in B. glabrata coding regions. The presence of DNA methylation in B. glabrata was also confirmed by several experimental approaches: restriction enzymatic digestion with isoschizomers, bisulfite conversion based techniques and LC-MS/MS analysis. Results In this work, we report that DNA methylation, which is one of the carriers of epigenetic information, occurs in B. glabrata; approximately 2% of cytosine nucleotides are methylated. We describe the methylation machinery of B. glabrata. Methylation occurs predominantly at CpG sites, present at high ratios in coding regions of genes associated with housekeeping functions. We also demonstrate by bisulfite treatment that methylation occurs in multiple copies of Nimbus, a transposable element. Conclusions This study details DNA methylation for the first time, one of the carriers of epigenetic information in B. glabrata. The general characteristics of DNA methylation that we observed in the B. glabrata genome conform to what epigenetic studies have reported from other invertebrate species.
    Full-text · Article · Jun 2013 · Parasites & Vectors
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    • "At the 3′ end, we found a poly-A tail, indicating that Rter is a fully processed transcript of RNA polymerase II. For Limi, the protein-based RepeatMasking analysis of the coding regions showed significant sequence similarities to the nimbus from Schistosoma manson [43], suggesting that Limi belonged to the a newly defined clade, Nimb. This clade has been recently recognised to be an independent clade, which included members from insects, molluscs, and fishes [44], [45]. "
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