DNA methylation analysis uncovers a fine-tuned regulation of expression of the polymeric Ig receptor gene in the Antarctic teleost Trematomus bernacchii

The polymeric immunoglobulin receptor (pIgR) is an evolutionary conserved transmembrane glycoprotein that mediates the transport of polymeric immunoglobulins across epithelial barriers, essential for protecting host mucosal surfaces from pathogens. Although the function of pIgR is well described in mammals and teleost fish, its gene structure and expression regulation yet remain elusive. Previously, we identified the gene encoding the pIgR in the cold-adapted teleost Trematomus bernacchii, belonging to the suborder Notothenioidei, a dominant component of Antarctic fish fauna. Comparative analysis of pIgR encoding sequences from different teleosts revealed structural features unique to Antarctic species. Among them, a CpG island was detected within the promoter region of the pIgR gene, where DNA methylation is known to occur and influence gene expression. In the present work, we report the presence of an additional CpG island located in the second intron, upstream of a DNA transposon motif. Since epigenetic regulation of genes from Antarctic fish is almost unexplored, we experimentally assessed the methylation status of both CpG islands in gills, gut and liver. The promoter CpG island showed varying methylation levels across different tissues, suggesting a regulation of the pIgR gene expression in a tissue-specific manner. Conversely, the intronic CpG island was highly methylated in all analyzed tissues, supporting the role of DNA methylation in controlling transposon activity. This study provides the first evidence of epigenetic modulation of an immune gene in an Antarctic teleost species, offering novel insights into gene regulation and adaptation to extreme cold environments.