Osmotic and ionic regulation by hololimnetic freshwater crustaceans: a molecular role for gill ion transporters

Abstract

AbstractOwing to their extraordinary niche diversity, the Crustacea are ideal for comprehending the evolution of osmoregulation. The processes that effect systemic hydro-electrolytic homeostasis maintain hemolymph ionic composition via membrane transporters located in highly specialized gill ionocytes. We evaluated physiological and molecular hyper- and hypo-osmoregulatory mechanisms in two phylogenetically distant, freshwater crustaceans, the crabDilocarcinus pageiand the shrimpMacrobrachium jelskii, when osmotically challenged for up to 10 days. When in distilled water, hemolymph osmolality and [Cl−] increased briefly inD. pagei, stabilizing at initial values, while [Na+] decreased continually. Gill V(H+)-ATPase, Na+/K+-ATPase and Na+/K+/2Cl−gene expressions were unchanged. InM. jelskii, hemolymph osmolality, [Cl−] and [Na+] decreased continually for 12 h, the shrimps no longer surviving. Gill transporter gene expressions increased 2- to 5-fold. After 10-days exposure to brackish water,D. pageiwas isosmotic, iso-chloremic and iso-natriuremic. Gill V(H+)-ATPase expression decreased while Na+/K+-ATPase and Na+/K+/2Cl−expressions were unchanged. InM. jelskii, the hemolymph was hypo-regulated, particularly [Cl−]. Transporter expressions initially increased 3- to 12-fold, declining to control values. Gill V(H+)-ATPase expression underlies the ability ofD. pageito survive in fresh water while Na+/K+-ATPase and Na+/K+/2Cl−expressions enableM. jelskiito deal with osmotic challenge. These findings reveal divergent responses in two unrelated crustaceans habiting a similar osmotic niche. WhileD. pageihas maintained the capacity to tolerate elevated cellular isosmoticity despite its inability to secrete salt,M. jelskiidisplays clear hypo-osmoregulatory ability. Each species has developed distinct strategies at the transcription and systemic levels during adaptation to fresh water.Summary statementDuring their evolutionary adaptation to fresh water, unrelated hololimnetic crustaceans have developed physiological strategies like tolerating elevated cellular isosmoticity or regulating hypo-osmoregulatory ability at the gene transcription level.