Comparative transcriptomic analysis of deep- and shallow-water barnacle species (Cirripedia, Poecilasmatidae) provides insights into deep-sea adaptation of sessile crustaceans

Abstract

Background

Barnacles are specialized marine organisms that differ from other crustaceans in possession of a calcareous shell, which is attached to submerged surfaces. Barnacles have a wide distribution, mostly in the intertidal zone and shallow waters, but a few species inhabit the deep-sea floor. It is of interest to investigate how such sessile crustaceans became adapted to extreme deep-sea environments. We sequenced the transcriptomes of a deep-sea barnacle, Glyptelasma gigas collected at a depth of 731 m from the northern area of the Zhongjiannan Basin, and a shallow-water coordinal relative, Octolasmis warwicki. The purpose of this study was to provide genetic resources for investigating adaptation mechanisms of deep-sea barnacles.

Results

Totals of 62,470 and 51,585 unigenes were assembled for G. gigas and O. warwicki, respectively, and functional annotation of these unigenes was made using public databases. Comparison of the protein-coding genes between the deep- and shallow-water barnacles, and with those of four other shallow-water crustaceans, revealed 26 gene families that had experienced significant expansion in G. gigas. Functional annotation showed that these expanded genes were predominately related to DNA repair, signal transduction and carbohydrate metabolism. Base substitution analysis on the 11,611 single-copy orthologs between G. gigas and O. warwicki indicated that 25 of them were distinctly positive selected in the deep-sea barnacle, including genes related to transcription, DNA repair, ligand binding, ion channels and energy metabolism, potentially indicating their importance for survival of G. gigas in the deep-sea environment.

Conclusions

The barnacle G. gigas has adopted strategies of expansion of specific gene families and of positive selection of key genes to counteract the negative effects of high hydrostatic pressure, hypoxia, low temperature and food limitation on the deep-sea floor. These expanded gene families and genes under positive selection would tend to enhance the capacities of G. gigas for signal transduction, genetic information processing and energy metabolism, and facilitate networks for perceiving and responding physiologically to the environmental conditions in deep-sea habitats. In short, our results provide genomic evidence relating to deep-sea adaptation of G. gigas, which provide a basis for further biological studies of sessile crustaceans in the deep sea.