Salt transport by the gill Na+-K+-2Cl− symporter in palaemonid shrimps: exploring physiological, molecular and evolutionary landscapes

• Published in: Comparative biochemistry and physiology. Part A, Molecular & integrative physiology Molecular & integrative physiology, 2021-07, Vol.257, p.110968-110968, Article 110968
• Main Authors: Maraschi, Anieli Cristina, Faria, Samuel Coelho, McNamara, John Campbell
• Format: Article
• Language: English
• Subjects: Acclimatization; Animals; Biological Evolution; Comparative phylogenetic methods; Ecosystem; Evolution of palaemonid shrimps; Female; Fresh Water; Gene and protein expression; Gill ion transporters; Gills - physiology; Hemolymph - metabolism; Ions; Kinetics; Male; Osmolar Concentration; Osmoregulation; Osmosis; Osmotic and chloride regulation; Palaemonidae - genetics; Palaemonidae - physiology; Phylogeny; RNA, Messenger - metabolism; Salinity; Sodium - metabolism; Sodium-Potassium-Exchanging ATPase - metabolism; Sodium‑potassium-two chloride transporter; Species Specificity; Symporters - genetics; Symporters - metabolism; Treatment Outcome; Water-Electrolyte Balance - physiology
• ISSN: 1095-6433; 1531-4332
• DOI: 10.1016/j.cbpa.2021.110968

Palaemonid shrimps inhabit osmotic niches from marine to continental waters. They hyper-regulate hemolymph osmolality and ionic concentrations in dilute media, hypo-regulating in concentrated media. Their gill epithelia express ion transporters like the Na+-K+-2Cl− symporter (NKCC) thought to play a role in salt secretion. To examine Cl− hypo-regulatory capability and phylogenetic correlations between gill NKCC mRNA levels and protein expression, we used palaemonids ranging from marine tide pools through estuaries (Palaemon) to coastal and continental fresh waters (Macrobrachium). We established the species' upper critical salinity limits (UL50) and short- (24 h) and long-term (120h) hypo-regulatory abilities at salinities of 80% of their UL50's (80%UL50). The Palaemon species exhibited the highest UL50's and greatest hypo-regulatory capabilities; among the Macrobrachium species, UL50's were higher in the diadromous than in the hololimnetic species. While basal transcript levels of gill NKCC mRNA were highest in P. pandaliformis, levels were unaffected by salinity or exposure time in all species. However, gill NKCC protein abundance increased after 120-h exposure at the 80%UL50 in all Macrobrachium species, except M. potiuna. Unexpectedly, hemolymph hyper-osmoregulatory capability in acclimatization media correlated with gill NKCC protein synthesis, while gill NKCC mRNA expression correlated with hemolymph hyper-Cl− regulation in Macrobrachium. These findings, together with the evolutionary history of osmoregulation in this shrimp clade, suggest a role for the gill NKCC symporter in both salt uptake and secretion. The evolution of NKCC protein expression responsiveness, unlike hemolymph hypo-regulation and NKCC mRNA expression, may have been driven by environmental salinity during niche radiation. While mRNA expression of the gill Na+-K+-2Cl− symporter is unchanged during acclimation of palaemonid shrimps to saline media, protein expression is up regulated, revealing a role in chloride secretion. [Display omitted] •UL50's and osmotic/Cl− hypo-regulatory ability are greater in Palaemon than Macrobrachium.•Salinity and exposure time have no effect on gill NKCC mRNA transcript levels.•Gill NKCC protein expression increases on high salinity challenge in Macrobrachium.•Hemolymph Cl−hyper-regulation correlates positively with gill NKCC mRNA expression.•Hemolymph osmolality hyper-regulation correlates with gill NKCC protein expression.•During palaemonid radiation