V-type H+-ATPase and Na+,K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation

Abstract

SUMMARY Because of their diverse habitats, crabs are excellent experimental species to study owing to the morphological changes and physiological adaptation that occur during their terrestrial invasion. Their hemolymphic osmoregulation in brackish water is crucial for a successful terrestrial invasion. Crabs can actively uptake or excrete ions upon salinity change, and the gills play a major role among the osmoregulatory organs. Several enzymes are involved in the osmoregulatory process, including Na+,K+-ATPase and V-type H+-ATPase (V-H+-ATPase). Na+,K+-ATPase is the driving force in establishing an ion gradient across the epithelial cell membrane in marine crabs. It has been reported that the osmoregulatory mechanisms in freshwater crabs are different from those in marine ones, suggesting that the driving force may come from V-H+-ATPase by generating the H+ ion gradient to facilitate the ion flow. Thirteen crab species from two families were used in this study. These crabs lived in five different habitats, including marine,intertidal, bimodal, freshwater and terrestrial habitats. The distribution of V-H+-ATPase in the 13 euryhaline crabs was revealed by histochemistry. V-H+-ATPase was localized in the apical region in crabs that could survive in the freshwater environment. We found that the freshwater and terrestrial crabs with stable Na+,K+-ATPase activity during salinity changes tended to have an apical V-H+-ATPase, whereas the intertidal ones with varying Na+,K+-ATPase activity showed a cytoplasmic V-H+-ATPase distribution. Finally, in Uca formosensis, a crab that had stable Na+,K+-ATPase activity, a significant difference in V-H+-ATPase activity between salinities was found. In conclusion, the hypothesis that V-H+-ATPase plays a crucial role in the freshwater adaptation of crabs is supported by our systemic investigation on 13 euryhaline crabs.

Effects of salinity acclimation and eyestalk ablation on Na+, K+, 2Cl− cotransporter gene expression in the gill of Portunus trituberculatus:a molecular correlate for salt-tolerant trait

“…NKCC is an integral membrane protein responsible for the simultaneous transport of one Na + , one K + , and two Cl − ions from the external to the internal side of epithelial cells (Kang et al 2010). Although previous studies suggest that NKCC plays a critical role in the osmoregulatory endurance of fish (Kang et al 2010;Watson et al 2014;LorinNebel et al 2006;Ip et al 2013;Chandrasekar et al 2014), its role in salinity adaptations has been little studied in crustaceans compared to other ion transport genes (i.e., Na + , K + -ATPase, V-type H + -ATPase, carbonic anhydrase (CA)) (Tsai and Lin 2007;Lucu et al 2008;Firmino et al 2011;Han et al 2015).…”

Roles of crustacean hyperglycaemic hormone in ionic and metabolic homeostasis in the Christmas Island Blue crabDiscoplax celeste

“…A subject of topical interest is the involvement of CHH in ionoregulatory processes (Charmantier-Daures et al, 1994;Charmantier et al, 1999;Chung et al, 1999;Townsend et al, 2001;Serrano et al, 2003;Chung and Webster, 2006). Whilst it is known that sinus gland extracts cause rapid and reversible changes in transepithelial potentials, and Na + transport in isolated perfused gills of Pachygrapsus marmoratus (Spanings-Pierrot et al, 2000), the precise mechanisms regulated by CHH in crustacean gill tissues remain poorly investigated, despite our extensive knowledge of branchial membrane exchangers and pumps (Lucu, 1990;Onken et al, 1991;Onken and Putzenlechner, 1995;Lucu and Towle, 2003;Weihrauch et al, 2004;Tsai and Lin, 2007;Masui et al, 2008). Additionally, because the insect equivalent of CHH-ion transport peptide (ITP) has long been known to stimulate water uptake in the locust hindgut by opening Cl -channels (Phillips and Audsley, 1995;Phillips et al, 1998), it is surprising that the ionoregulatory processes controlled by CHH have not attracted further interest.…”

Evolutionary transition to freshwater by ancestral marine palaemonids: evidence from osmoregulation in a tide pool shrimp

“…Consequently, freshwater species must expend more energy on the anisosmotic and anisoionic regulatory mechanisms that maintain their steep osmotic and ionic gradients against the surrounding medium, sustaining their essential life processes. The successful invasion of dilute media includes the selection of favorable morphological (Taylor & Taylor 1992, Onken & McNamara 2002, physiological (Péqueux 1995, Kirschner 2004, Weihrauch et al 2004, Tsai & Lin 2007, Freire et al 2008 and biochemical (Leone et al 2005, Mendonça et al 2007) adaptations, and those ancestral crustaceans that surmounted this barrier evidently evolved efficient mechanisms of hyperosmotic and ionic regulation, allowing survival in such habitats (Schubart & Diesel 1998.…”