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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 replicated events of deep-sea colonization (288 individuals from 216 species). We found consistent signatures of molecular convergence in functions related to protein biogenesis, including protein folding and translation. Five genes were recurrently positively selected, including chaperonin-containing TCP-1 subunit α (CCTα), which is essential for protein folding. Molecular convergence was detected at the functional and gene levels but not at the amino-acid level. Pressure-adapted proteins are expected to display higher stability to counteract the effects of denaturation. We thus examined in silico local protein stability of CCTα across the ophiuroid tree of life (967 individuals from 725 species) in a phylogenetically corrected context and found that deep-sea-adapted proteins display higher stability within and next to the substrate-binding region, which was confirmed by in silico global protein stability analyses. This suggests that CCTα displays not only structural but also functional adaptations to deep-water conditions. The CCT complex is involved in the folding of ∼10% of newly synthesized proteins and has previously been categorized as a "cold-shock" protein in numerous eukaryotes. We thus propose that adaptation mechanisms to cold and deep-sea environments may be linked and highlight that efficient protein biogenesis, including protein folding and translation, is a key metabolic deep-sea adaptation.
Fig. 1. Workflow used in this study. (A) Schematic representation of the phylogeny of Ophiuroidea (redrawn from Christodoulou et al. [2019]). Four families (288 individuals from 216 species) with a shallow-water common ancestor and extant species in shallow (0â200âm) and deep (>200âm) environments are highlighted in different colors. The width of each triangle is proportional to the sampled number of species in each family. Ophiomyxidae (blue), Ophiodermatidae (green), Amphiuridae (pink), and Ophiotrichidae (yellow). (B) For each family (number of species used in brackets) and each one of the 416 single-copy orthologs, maximum-likelihood (ML) reconstructions were performed. Trees are drawn for illustration only with the branches of shallow-water (0â200âm) species colored in black and deep-water (>200âm) species in blue. (C) For each resulting ML tree, deep species were labeled as foreground branches and four positive selection detection methods were used (BUSTED, aBSREL, MEME, and MNM). To detect and exclude candidate genes displaying relaxation of selection, that is, accumulation of substitutions not due to increased selection pressure, the method RELAX was used. The final set of candidate genes for each family encompassed genes positively selected in at least three methods and not displaying relaxation of selection. Convergent evolution was examined by overlapping candidate genes per family. For the most interesting candidate gene, amino-acid convergence and tertiary structure analyses were performed, and protein stability profiles and global protein stability were calculated.
Fig. 3. Primary structure of CCTα. Ligand binding sites (PL, AH, and H11), ATP-binding sites, positively selected sites (method MEME), and sites displaying different local stability values between shallow and deep species (method phylANOVA) are highlighted. The sequence of the shallow-water Amphiuridae Amphiura constricta is used as template.
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