Primary amino acid sequences of decapod (Na+, K+)-ATPase provide evolutionary insights into osmoregulatory mechanisms

• Published in: Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2024-10, Vol.296, p.111696, Article 111696
• Main Authors: Fabri, Leonardo M., Moraes, Cintya M., Garçon, Daniela P., McNamara, John C., Faria, Samuel C., Leone, Francisco A.
• Format: Article
• Language: English
• Subjects: (Na+, K+)-ATPase; Amino Acid Sequence; Animals; Decapoda - enzymology; Decapoda - genetics; Decapoda - physiology; Domain; Evolution, Molecular; Gills - enzymology; Gills - metabolism; Motifs; Osmoregulation; Osmoregulation - genetics; Ouabain sensitivity; Phylogeny; Sodium-Potassium-Exchanging ATPase - chemistry; Sodium-Potassium-Exchanging ATPase - genetics; Sodium-Potassium-Exchanging ATPase - metabolism
• ISSN: 1095-6433; 1531-4332; 1531-4332
• DOI: 10.1016/j.cbpa.2024.111696

Decapod Crustacea exhibit a marine origin, but many taxa have occupied environments ranging from brackish to fresh water and terrestrial habitats, overcoming their inherent osmotic challenges. Osmotic and ionic regulation is achieved by the gill epithelia, driven by two active ATP-hydrolyzing ion transporters, the basal (Na+, K+)-ATPase and the apical V(H+)-ATPase. The kinetic characteristic of gill (Na+, K+)-ATPase and the mRNA expression of its α subunit have been widely studied in various decapod species under different salinity challenges. However, the evolution of the primary structure has not been explored, especially considering the functional modifications associated with decapod phylogeny. Here, we proposed a model for the topology of the decapod α subunit, identifying the sites and motifs involved in its function and regulation, as well as the patterns of its evolution assuming a decapod phylogeny. We also examined both the amino acid substitutions and their functional implications within the context of biochemical and physiological adaptation. The α-subunit of decapod crustaceans shows greater conservation (∼94% identity) compared to the β-subunit (∼40%). While the binding sites for ATP and modulators are conserved in the decapod enzyme, the residues involved in the α-β interaction are only partially conserved. In the phylogenetic context of the complete sequence of (Na+, K+)-ATPase α-subunit, most substitutions appear to be characteristic of the entire group, with specific changes for different subgroups, especially among brachyuran crabs. Interestingly, there was no consistent separation of α-subunit partial sequences related to habitat, suggesting that the convergent evolution for freshwater or terrestrial modes of life is not correlated with similar changes in the enzyme's primary amino acid sequence. Topology of gill (Na+, K+)-ATPase highlighting the amino acid residue substitutions shown in a decapod phylogeny. [Display omitted] •The decapod (Na+, K+)-ATPase α-subunit shows greater conservation than β-subunit.•The binding sites for ATP and modulators are conserved in the decapod enzyme.•Most substitutions of α-subunit emerged at the onset of the Decapoda lineage.•Convergent evolution for freshwater life is not linked to similar sequence changes.•Substitution at TM1–2 may cause lower sensitivity to ouabain in decapods.