Convergent evolution and structural adaptation in the eukaryotic chaperonin CCTα of deep-sea brittle stars

The deep ocean is the largest biome on Earth and yet it is among the least studied environments of our planet. Life at great depths requires several specific adaptations, however their molecular mechanisms remain understudied. We examined patterns of positive selection in 416 genes from four brittle star (Ophiuroidea) families displaying independent events of deep-sea colonization (288 individuals from 216 species). We found consistent signatures of molecular convergence in five genes, including the CCTα gene (Chaperonin Containing TCP-1 subunit α), which is a subunit of the key eukaryotic chaperonin CCT involved in the folding of ~10% of newly synthesized proteins, notably the cytoskeletal proteins actin and tubulin. We did not find signatures of convergence in amino-acid profiles, and positively selected sites were different among families, together indicating that convergence was detected at the gene but not at the amino-acid level in CCTα. Pressure-adapted proteins are expected to display higher stability to counter-interact the effects of denaturation. We thus examined in silico protein stability profiles of CCTα across the ophiuroid tree of life (967 individuals from 725 species) in a phylogenetically-corrected context and found that depth-adapted proteins display higher stability within and next to the substrate-binding region, suggesting that this gene displays not only structural but also functional adaptations to deep water conditions. CCT, the most complex eukaryotic chaperonin, has previously been categorized as cold-shock protein in numerous organisms. Furthermore, accelerated evolution of cold-shock proteins or expansion of these families has been shown for several deep-sea species. We thus propose that adaptation mechanisms to cold and deep-sea environments may be linked and highlight that efficient protein folding is a key metabolic deep-sea adaptation.