1. Convergent Evolution and Structural Adaptation to the Deep Ocean in the Protein-Folding Chaperonin CCTα
- Author
-
Andrew F. Hugall, Alexandra Anh-Thu Weber, and Timothy D. O'Hara
- Subjects
AcademicSubjects/SCI01140 ,0106 biological sciences ,Oceans and Seas ,Protein subunit ,In silico ,Adaptation, Biological ,Biology ,010603 evolutionary biology ,01 natural sciences ,Chaperonin ,Starfish ,TCP-1 ,03 medical and health sciences ,positive selection ,protein folding ,Convergent evolution ,Genetics ,Animals ,Denaturation (biochemistry) ,14. Life underwater ,Selection, Genetic ,Gene ,Ecology, Evolution, Behavior and Systematics ,pressure adaptation ,030304 developmental biology ,0303 health sciences ,TC P-1 ,Protein Stability ,AcademicSubjects/SCI01130 ,Biological Evolution ,protein stability ,Evolutionary biology ,Protein folding ,Chaperonin Containing TCP-1 ,Biogenesis ,Extreme Environments ,Research Article ,Echinodermata - Abstract
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.
- Published
- 2020