Diversity of sponge mitochondrial introns revealed by cox 1sequences of Tetillidae

Abstract

BackgroundAnimal mitochondrial introns are rare. In sponges and cnidarians they have been found in the cox 1 gene of some spirophorid and homosclerophorid sponges, as well as in the cox 1 and nad 5 genes of some Hexacorallia. Their sporadic distribution has raised a debate as to whether these mobile elements have been vertically or horizontally transmitted among their hosts. The first sponge found to possess a mitochondrial intron was a spirophorid sponge from the Tetillidae family. To better understand the mode of transmission of mitochondrial introns in sponges, we studied cox 1 intron distribution among representatives of this family.ResultsSeventeen tetillid cox 1 sequences were examined. Among these sequences only six were found to possess group I introns. Remarkably, three different forms of introns were found, named introns 714, 723 and 870 based on their different positions in the cox 1 alignment. These introns had distinct secondary structures and encoded LAGLIDADG ORFs belonging to three different lineages. Interestingly, sponges harboring the same intron form did not always form monophyletic groups, suggesting that their introns might have been transferred horizontally. To evaluate whether the introns were vertically or horizontally transmitted in sponges and cnidarians we used a host parasite approach. We tested for co-speciation between introns 723 (the introns with the highest number of sponge representatives) and their nesting cox 1 sequences. Reciprocal AU tests indicated that the intron and cox 1 tree are significantly different, while a likelihood ratio test was not significant. A global test of co-phylogeny had significant results; however, when cnidarian sequences were analyzed separately the results were not significant.ConclusionsThe co-speciation analyses thus suggest that a vertical transmission of introns in the ancestor of sponges and cnidarians, followed by numerous independent losses, cannot solely explain the current distribution of metazoan group I introns. An alternative scenario that includes horizontal gene transfer events appears to be more suitable to explain the incongruence between the intron 723 and the cox 1 topologies. In addition, our results suggest that three different intron forms independently colonized the cox 1 gene of tetillids. Among sponges, the Tetillidae family seems to be experiencing an unusual number of intron insertions.

Evolution of group I introns in Porifera: new evidence for intron mobility and implications for DNA barcoding

“…Fungi are proposed as the primary donor of mt group I introns not only in plants (e.g., [14]), but also in cnidarians [31] and sponges [47, 65, 82]. Placozoa have also been suggested as possible donors in sponges, but only for intron 387 in one species [48].…”

Evolutionary and biogeographical implications of degraded LAGLIDADG endonuclease functionality and group I intron occurrence in stony corals (Scleractinia) and mushroom corals (Corallimorpharia)

“…This contrasts with the general assumption that introns inserted in different positions are phylogenetically not closely related [36]. The exclusive vertical intron transfer proposed for robust Scleractinia is in disagreement with the widely accepted combined horizontal/vertical transfer mechanisms shown in sponges and sea anemones [22,23,25,26]. Moreover, the study of Fukami et al did not include corals of complex Scleractinia, which contains some of the most important and widespread reef-building coral families [33].…”

The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics

“…Order Zoanthidea Savalia savaglia DQ825686 1238 *The cox1 group I intron has been found in five additional black coral taxa -see Supporting Information Table S8. the intron share yet another insertion site with the sponges Plakinastrella Schulze, 1880 and Cinachyrella Wilson, 1925(Szitenberg et al, 2010. Among the other black corals with the cox1 intron, we sequenced 544 bp of the 3′-end of the intron in S. litocrada (specimen FEL604-47-2), P. pennacea (USNM 1086297) and M. ulex (TMOa0406L-6) (sequence data corresponding to the 5′-end of the intron were not obtained).…”