Abstract
According to the tRNA punctuation model, the mitochondrial genome (mtDNA) of mammals and arthropods is transcribed as large polycistronic precursors that are maturated by endonucleolytic cleavage at tRNA borders and RNA polyadenylation. Starting from the newly sequenced mtDNA of Ixodes ricinus and using a combination of mitogenomics and transcriptional analyses, we found that in all currently-sequenced tick lineages (Prostriata, Metastriata and Argasidae) the 3′-end of the polyadenylated nad1 and rrnL transcripts does not follow the tRNA punctuation model and is located upstream of a degenerate 17-bp DNA motif. A slightly different motif is also present downstream the 3′-end of nad1 transcripts in the primitive chelicerate Limulus polyphemus and in Drosophila species, indicating the ancient origin and the evolutionary conservation of this motif in arthropods. The transcriptional analyses suggest that this motif directs the 3′-end formation of the nad1/rrnL mature RNAs, likely working as a transcription termination signal or a processing signal of precursor transcripts. Moreover, as most regulatory elements, this motif is characterized by a taxon-specific evolution. Although this signal is not exclusive of ticks, making a play on words it has been named “Tick-Box”, since it is a check mark that has to be verified for the 3′-end formation of some mt transcripts, and its consensus sequence has been here carefully characterized in ticks. Indeed, in the whole mtDNA of all ticks, the Tick-Box is always present downstream of nad1 and rrnL, mainly in non-coding regions (NCRs) and occasionally within trnL(CUN). However, some metastriates present a third Tick-Box at an intriguing site - inside the small NCR located at one end of a 3.4 kb translocated region, the other end of which exhibits the nad1 Tick-Box - hinting that this motif could have been involved in metastriate gene order rearrangements.
Highlights
Chelicerates constitute a major lineage within Arthropoda and encompass taxa of evolutionary interest, such as the deepbranching lineage Xiphosura, and species of medical relevance, such as the Arachnida
After a brief summary of the main features of the I. ricinus mtDNA, we describe the identification of a degenerate 17 bp sequence motif directing the 39-end formation of nad1 and rrnL transcripts in all major tick lineages
Since it is shared with L. polyphemus, this organization is considered to be ancestral to all arthropods [10,11,52]
Summary
Chelicerates constitute a major lineage within Arthropoda and encompass taxa of evolutionary interest, such as the deepbranching lineage Xiphosura (including the living fossil Limulus polyphemus), and species of medical relevance, such as the Arachnida (e.g. ticks, mites, scorpions, spiders). Ticks (Ixodida) are obligate bloodsucking ectoparasites that originated in early/middle Permian (300–260 million years ago, Mya) [1,2,3] and parasitize a variety of terrestrial vertebrates [4,5]. The sheep tick Ixodes ricinus (Linnaeus 1758), the most common blood-feeding ectoparasite in Europe, is the vector of Lyme disease and other bacteria, protozoa and viruses [8]. I. ricinus is of particular interest in that it harbours a symbiont, ‘‘Candidatus Midichloria mitochondrii’’ [9], that resides in the intermembrane space of mitochondria. It can be considered a model of a three-levels relationship: the vertebrate host, the tick ectoparasite, and the intra-mitochondrial bacterium ‘‘Candidatus M. mitochondrii’’
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