Lost IgT gene in icefish: another chapter of the evolutionary tale of Antarctic fish

Notothenioidei is a monophyletic lineage that accounts for the majority of teleost fish fauna living in the freezing sea of the Southern Ocean. They are an amazing example of adaptive radiation and an interesting model for the study of cold adaptation. During their evolutionary history, Antarctic fish have undergone significant genome alterations, as also highlighted in a previous work on the gene encoding the IgT heavy chain, lacking most of the second constant exon (CH2). A reconstruction across notothenioid phylogeny revealed that the partial loss of CH2 was shared by representative species from four Antarctic families along with the nearest non-Antarctic sister species Eleginops maclovinus. The present work is aimed at investigating Channichthyidae, since remaining the only family apparently lacking the entire IgT gene. The survey of available genomes and trascriptomes for this family revealed a heterogeneous situation, with some species (most notably Chionodraco, Cryodraco and Chaenodraco spp.) having entirely lost the IgT gene and others displaying a remnant pseudogene carrying only TM exons and a part of the upstream intron. Since the IgT gene was present and complete in all the other closely related taxa (Bathydraconinae, Cignodraconinae and Gymnodraconinae), the timing of the gene loss can be inferred to be coincident with the loss of red blood cells and hemoglobin occurred in the family. To evaluate how the two other evolutionary conserved isotypes can functionally compensate for the loss of IgT, tissue-specific expression of C. hamatus IgM and IgD was performed by qPCR, including T. bernacchii for comparison. IgM was found to be the predominant isotype expressed in icefish mucosal tissues. In particular, abundant IgM expressing cells were found in the lamina propria of the posterior intestine, as indicated by in situ hybridization analysis. Conversely, IgD transcripts were found to be predominantly expressed in the lymphoid organs. Of note, the expression levels of IgM in the intestine and of IgD in head kidney of C. hamatus were respectively 6- and 20-fold higher than in T. bernacchii tissues. As expected, IgT was the highest expressed isotype detected in mucosal tissues of T. bernacchii. Overall, the preliminary results presented here pave the way for completing the reconstruction of the evolutionary history of the IgT gene in Antarctic fish, culminated with its loss in icefish.