The evolutionary puzzle of IgT genes in antarctic fishes

The Perciform suborder Notothenioidei represents the major component of the Antarctic fish fauna, comprising five Antarctic families, Channichthydae, Bathydraconidae, Artedidraconidae, Nototheniidae, and Harpagiferidae, and three non-Antarctic families, Bovichtidae, Pseudaphritidae, and Eleginopidae. Notothenioids have evolved a variety of peculiar anatomical, physiological and biochemical features to adapt to the extremely cold Antarctic environment, providing an extraordinary model system to identify gene changes and investigate their importance for adaptive evolution. We have previously isolated and characterized IgT heavy chain constant region gene of the Antarctic teleost Trematomus bernacchii (family Nototheniidae), discovering that T. bernacchii IgT lack almost the entire heavy chain second constant domain, retaining only a few of amino acid residues. By analyzing cDNA sequences encoding IgT heavy chain three differently sized IgT transcript variants were identified, named Long, Short, and Shortest, 51-bp, 33-bp, 42-bp long, respectively. The aim of the present study is to provide a framework for understanding the loss of the CH2 domain through the notothenioid phylogeny. To this end, we isolated and characterized IgT genes from other species belonging to families Nototheniidae, Bathydraconidae and Artedidraconidae. In all cases the remnant CH2 exon preserved the donor and acceptor splicing sites to be correctly spliced into the mature transcript, giving rise to different cDNA variants: 24-51 bp long (8-17 aa) according to the species analyzed. Moreover, one representative each of the two non-Antarctic families was included in our studies for comparison: Eleginops maclovinus (family Eleginopidae), and Bovichtus diacanthus, (family Bovichtidae). Both diverged early from the main notothenioid lineage, before a severe decrease in water temperature and climatic and geographic isolation of Antarctica. A comparative analysis at genomic level has highlighted that the remnant CH2 exon is shared by all Antarctic fish families analyzed in the present work. Amazingly, the loss of most CH2 is shared also by E. maclovinus but not by B. diacanthus. These results may help shed light on the evolutionary processes that underlie the origins of such gene modifications.