Identification and isolation of a retrotransposon from the freshwater sponge Lubomirskia baicalensis: implication in rapid evolution of endemic sponges.

Abstract

Transposons are mobile genetic elements that are found in all major branches of life. Similarities to retroviruses concerning genome structure and transposition mechanism suggest a familial relationship. Transposons are important evolutionary drivers that trigger genetic changes such as genomic rearrangement, alteration of gene expression, and gene duplication. And, indeed, now more than ever the effect of transposons on genome evolution represents a dynamic field of research. Since sponges (phylum Porifera) are the phylogenetically oldest still extant metazoan taxon, the study of poriferan mobile elements contributes to the understanding of the generation of phenotypic diversity and speciation at the base of the metazoan tree of life. This work describes the analyses of the first poriferan mobile genetic element so far identified, the long terminal repeats- retrotransposon Baikalum-1 of Lubomirskia baicalensis (Demospongiae; Ceractinomorpha). Baikalum-1 embraces a continuous open reading frame, putatively coding for a polyprotein that consists of nucleo capsid, protease, reverse transcriptase, RNase H, and integrase, all proteins/ enzymes characteristic of retrotransposons. Baikalum-1 was discovered in all freshwater sponge species endemic to Lake Baikal, as well as in cosmopolitan sponge species that inhabit a Lake Baikal-feeding rivulet. However, the same cosmopolitan species sampled from lakes and rivers (Siberian and European) with no direct contact to Lake Baikal did not contain this particular mobile genetic element. Thus, Baikalum-1 is probably the result of an evolutionarily ancient retroviral infection that spread exclusively amongst Baikalian sponge species. In addition, the retro-transposon is found in the vicinity of the silicatein-A1 gene. Silicateins are cathepsin-like proteins that catalyze the synthesis of poriferan siliceous skeletal elements (spicules). In L. baicalensis, the silicatein-A1 gene is flanked by two palindroms, probably remnants of transposons that might be responsible for the emergence of four different silicatein genes, uniquely present in freshwater but not marine sponges. Adaptation of sponges to the freshwater habitat (with its significantly higher silica content compared to the marine milieu) required the ability to evolve rapidly, which could be conferred by high transpositional activity, accompanied by duplication and diversification of the ancestral silicatein gene of marine species.