Introduction
Transposable elements (TEs), better known as transposons or “jumping genes”, are dispersed, repetitive DNA segments able to move and insert autonomously in the genome through copy-and-paste RNA (class I retrotransposons) or cut-and-paste DNA mechanisms (class II transposons) (Finnegan, 1989). TEs account for most of the vertebrate genome and, although long dismissed as “junk DNA”, they have fuelled events such as speciation, de-novo gene birth and large-scale chromosomal rearrangements (Auvinet et al., 2018; Long et al., 2003; Lönnig & Saedler, 2002). However, uncontrolled mobilisation of TEs can compromise genome integrity, and trigger chronic inflammation or even tumourigenesis through persistent activation of transcription factors such as NF-κB and p53 (Gudkov et al., 2011). In this sense, epigenetic locks such as methylation and acetylation are able to keep TEs silent (Saul & Kosinsky, 2021). In addition, the immune system is able to operate as a second surveillance mechanism whereby, when epigenetic silencing fails, TE-derived nucleic acids accumulate in the cytoplasm. Then, they are able to mimic viral signatures and activate canonical DNA/RNA sensors such as Toll-like receptors, triggering type I interferon and pro-inflammatory cytokine responses that restrain further mobilisation (Rakoff-Nahoum & Medzhitov, 2009). In this context, teleost fishes are particularly noteworthy for harbouring the largest repertoire of TEs known to date, while possessing the earliest and most fully developed combination of innate and adaptive immune defences among vertebrates (Swain & Nayak, 2009). Nevertheless, the critical relationship between TEs and immune system, potentially central to understanding TE activity and its consequences, remains largely unexplored in fish species.
Material and Methods
Canonical TEs consensus sequences for eight cultured teleosts—zebrafish (Danio rerio), green pufferfish (Tetraodon nigroviridis), Japanese medaka (Oryzias latipes), European seabass (Dicentrarchus labrax), rainbow trout (Oncorhynchus mykiss), European eel (Anguilla anguilla), Nile tilapia (Oreochromis niloticus) and gilthead seabream (Sparus aurata)—were retrieved from FishTEDB. Each species-specific library was imported into OmicsBox software (v. 3.4.5) and launched as a BLASTn query (E-value ≤ 1 x 10⁻¹⁰) against the full Actinopterygii section of GenBank. The resulting hit tables were inspected manually, and for every TE, we flagged alignments whose first (highest-scoring, longest) match overlapped a locus annotated as immune-related (e.g., tlr, nlr, ifn, complement, cytokine, antiviral genes, etc.) and discarded the rest to avoid redundancies produced by long consensus sequences. For each retained TE-immune pair we recorded TE class/superfamily, alignment coverage (% query length) and identity; matched immune gene names were cross-checked in UniProt to confirm their immune function. Curated lists were then collated by species to expose shared versus lineage-specific patterns.
Results and Discussion
The screen yielded 333 robust TE–immune contacts distributed among the eight species. Most insertions clustered in membrane-bound pathogen-recognition receptors (Toll-like, complement and assorted cytokine receptors), cytosolic inflammasome sensors of the NLR-PYD/CARD family, and antiviral effectors such as type-I interferons, and Mx proteins. hAT, Tc1-Mariner, and L2- and L1-type LINEs lineages dominated, underscoring repeated involvement of both DNA-transposon and retrotransposon and classes in shaping immune loci. Based on these results, we hypothesize that TE fragments persisting in regulatory or coding regions of membrane receptors could have been selectively retained whenever they conferred improved pathogen detection or signalling capacity, thereby driving the expansion and functional diversification of innate-immune receptors in fish (Krasnov et al., 2005). Incomplete insertions—such as the TE fragment within tlr9 of rainbow trout—could likewise function as inducible regulatory modules, adding an extra layer of epigenetic control (Ortega-Villaizan et al., 2009). Altogether, the observed pattern could be consistent with a scenario in which TE-driven genetic variation helps teleosts adapt to pathogen-rich aquatic habitats.
In conclusion, this multi-species in-silico survey uncovers a widespread presence of TE across key innate-immune pathways of eight farmed teleosts, underlining mobile DNA as a silent architect of fish immune evolution. Therefore, our results offer a new insight into the relationship between ET and the immune system that may be key to the search for genomic markers and the development of new vaccines in aquaculture.
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Acknowledgements
This work was supported by the Juan de la Cierva postdoctoral fellowship (JDC2023-052846-I) funded by MICIU/AEI/10.13039/501100011033 and co-financed by the European Social Fund Plus (FSE+).