Taxonomic distribution of Mitochondrial introns

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Introduction

Taxonomic distribution of mitochondrial introns

Mitochondrial introns are mobile genetic elements capable of autonomous propagation in the their host's cells [1–3]. They encode homing endonuclease and maturase (Group I introns) or reverse transcriptase (Group II introns) domains that catalyse their mobility [4,5]. Mitochondrial introns are rare in Metazoa. They have been found in Placozoa (Group I and II), Cnidaria, Porifera (Group I only) and Annelida (Group II only). Within these phyla, they were sporadically encountered in unrelated families [6–15].

As for Metazoa in general, mitochondrial introns in sponges, all belonging to Group I, are considered rare. This has been based on their discovery in cox1 fragments of only two families from different sponge classes [12–14,16], as well as the low proportion of complete sponge mitochondrial genomes possessing such introns (3 out of 51 GenBank records, release 201.0, accessed June 8th 2014). Their sparsity in sponges served as one of the lines of evidence supporting their horizontal gene transfer (HGT). Other evidences included the phylogenetic incongruence between the introns and their sponge hosts and the phylogenetic relationship of the introns' ORFs to those of fungi introns [12,14]. However, these evidences were not always perceived as proof of HGT [13], mainly due to an apparent correlation in the evolutionary rates of the intron and cox1 sequences.

Implications on cox1 barcoding

Two of the mitochondrial intron forms found in sponges are inserted in positions that are located within the reverse Folmer fragment primer region. In a few cases, it is possible to say with confidence that the presence of an intron prevented the successful amplification of the standard Folmer fragment. Rot et al. [12] identified the first poriferan intron, in Cinachyrella levantinensis (Tetilla sp. sensu Ilan [17]), using an alternative reverse primer, after failing to amplify the Folmer fragment. In another case, Cárdenas et al. [18] have reported to have failed in amplifying the Folmer fragment in Cinachyrella alloclada, using a specimen in which the presence of an intron was confirmed later [14]. However, the total number of such failures is not accounted for since they are seldom reported. As a result, we cannot estimate the proportion of accepted poriferan species that have no cox1 barcode representation due to the presence of a mitochondrial intron, as we are in fact ignorant of the true prevalence of Group I introns in sponges.

Characteristics of poriferan Group I introns

Three different forms of Group I introns have been found in sponges, within the spirophorid family Tetillidae [14] and the homosclerophorid family Plakinidae [13]. The poriferan introns comprise three distinct forms denoted by the sequence position in which they are inserted. The numbers of the positions in the cox1 sequence of Amphimedon queenslandica (714, 723 and 870), which are homologous to intron insertion sites in other species, were used to name the different intron forms (i.e., intron 714, intron 723 and intron 870), for the sake of uniformity. A. queenslandica was adopted as reference, being the only species with a complete sequenced cox1 ORF at the time, although its cox1 sequence does not possess an intron [14]. Intron forms sharing an insertion site, have been found to share ORFs and secondary structures as well. However, these two features vary considerably among intron forms [14]. The taxonomic distribution of the three intron forms does not correspond the the sponges' phylogenetic relationships [14,19]. Introns 714 and 723 were found in Tetillidae, as well as in Plakinidae. Intron 870 was found so far only in Tetillidae [13,14]. However, some more recently identified plakinid introns, which were not yet characterized [16], are candidates to belong to this intron form.

In this study we have surveyed the representation of intron insertion sites, vacant and occupied, in the available cox1 sequence data, in order to estimate the impact of mitochondrial introns on the taxonomic representation of sponges in the global cox1 sequence barcode dataset. Our findings show that some sponge orders are under-represented, possibly because of unsuccessful attempts to amplify their cox1 gene, due to the presence of an intron. We present new sequence data that confirms the presence of introns in at least to orders in which they were not previously encountered. These two orders are indeed under-represented by the cox1 barcode sequence. This suggests that introns are more abundant the we have originally assumed and that vertical inheritance may have played a bigger role in their taxonomic distribution than we have previously concluded.

Material and methods

samples and molecular manipulations

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