Transcriptional Contribution of Transposable Elements in Relation to Salinity Conditions in Teleosts and Silencing Mechanisms Involved

Abstract

Fish are an interesting taxon comprising species adapted to a wide range of environments. In this work, we analyzed the transcriptional contribution of transposable elements (TEs) in the gill transcriptomes of three fish species exposed to different salinity conditions. We considered the giant marbled eel Anguilla marmorata and the chum salmon Oncorhynchus keta, both diadromous, and the marine medaka Oryzias melastigma, an euryhaline organism sensu stricto. Our analyses revealed an interesting activity of TEs in the case of juvenile eels, commonly adapted to salty water, when exposed to brackish and freshwater conditions. Moreover, the expression assessment of genes involved in TE silencing mechanisms (six in heterochromatin formation, fourteen known to be part of the nucleosome remodeling deacetylase (NuRD) complex, and four of the Argonaute subfamily) unveiled that they are active. Finally, our results evidenced for the first time a krüppel-associated box (KRAB)-like domain specific to actinopterygians that, together with TRIM33, might allow the functioning of NuRD complex also in fish species. The possible interaction between these two proteins was supported by structural prediction analyses.

Keywords: Krüppel-associated box domain zinc finger proteins (KRAB-ZFPs); fish; salinity; silencing mechanisms; transposable elements.

Figure 1

Transcriptional contribution of transposable elements in Anguilla marmorata, Oryzias melastigma, and Oncorhynchus keta gill transcriptomes. FW: freshwater; BW: brackish water; SW: salt water.

Figure 2

Transcriptional activity of Argonaute genes in Anguilla marmorata, Oryzias melastigma, and Oncorhynchus keta gill transcriptomes. FW: freshwater; BW: brackish water; SW: salt water.

Figure 3

Transcriptional activity of genes involved in heterochromatin formation in Anguilla marmorata, Oryzias melastigma, and Oncorhynchus keta gill transcriptomes. FW: freshwater; BW: brackish water; SW: salt water.

Figure 4

Transcriptional activity of NuRD complex genes in Anguilla marmorata, Oryzias melastigma, and Oncorhynchus keta gill transcriptomes. FW: freshwater; BW: brackish water; SW: salt water.

Figure 5

Multiple sequence alignment and 3D structures of the KRAB domain contained in the KRAB-like protein and that of TRIM33 protein. (A) In the upper side, a schematic representation of the domain architecture is reported for the A. marmorata TRIM33 protein. In the lower side, multiple sequence alignment related to the coiled-coil region of Homo sapiens TRIM28 protein and of ten actinopterygian TRIM33 sequences is showed. The main interacting residues at the interface are highlighted in orange. (B) In the upper side, a schematic representation of the domain architecture is reported for the Anguilla marmorata KRAB-like protein. In the lower side, the N-terminal region multiple sequence alignment of ten actinopterygian KRAB-like sequences is reported. (C) Ribbon and surface representation of A. marmorata TRIM33 structural model. Chain A and chain B are colored in dark and light orange, respectively. (D) Ribbon and surface representation of the putative A. marmorata KRAB-like domain. (E) Ribbon and surface representation of docked TRIM33/KRAB-like complex with a zoom on the residues H370/K373/I374/F377.

Figure 6

Transcriptional activity of KRAB-like and TRIM33 genes in Anguilla marmorata, Oryzias melastigma, and Oncorhynchus keta gill transcriptomes. FW: freshwater; BW: brackish water; SW: salt water.