Comprehensive analysis of genes contributing to euryhalinity in the bull shark, Carcharhinus leucas; Na+-Cl− co-transporter is one of the key renal factors up-regulated in acclimation to low-salinity environment in bull sharks, but not in houndsharks, Triakis scyllium

Abstract

Comprehensive analysis of genes contributing to euryhalinity in the bull shark, Carcharhinus leucas; Na + -Cl − co-transporter is one of the key renal factors upregulated in acclimation to low-salinity environment ABSTRACT Most cartilaginous fishes live principally in seawater (SW) environments, but a limited number of species including the bull shark, Carcharhinus leucas, inhabit both SW and freshwater (FW) environments during their life cycle. Euryhaline elasmobranchs maintain high internal urea and ion levels even in FW environments, but little is known about the osmoregulatory mechanisms that enable them to maintain internal homeostasis in hypoosmotic environments. In the present study, we focused on the kidney because this is the only organ that can excrete excess water from the body in a hypoosmotic environment. We conducted a transfer experiment of bull sharks from SW to FW and performed differential gene expression analysis between the two conditions using RNA-sequencing. A search for genes upregulated in the FW-acclimated bull shark kidney indicated that the expression of the Na + -Cl − cotransporter (NCC; Slc12a3) was 10 times higher in the FW-acclimated sharks compared with that in SW sharks. In the kidney, apically located NCC was observed in the late distal tubule and in the anterior half of the collecting tubule, where basolateral Na + /K + -ATPase was also expressed, implying that these segments contribute to NaCl reabsorption from the filtrate for diluting the urine. This expression pattern was not observed in the houndshark, Triakis scyllium, which had been transferred to 30% SW; this species cannot survive in FW environments. The salinity transfer experiment combined with a comprehensive gene screening approach demonstrates that NCC is a key renal protein that contributes to the remarkable euryhaline ability of the bull shark.

Tissue and salinity specific Na+/Cl− cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)

“…The expression of the sea lamprey ncca in both the gills and kidney of FW-acclimated sea lamprey is particularly interesting because, in teleost fishes, the NCC in the gills (NCC2) and kidney (NCC1) are two distinct NCC isoforms 33 , 35 , 37 . It is important to note that the elasmobranch NCC also exhibits FW-specific function in the gills and kidney 34 , 59 , similar to the expression pattern of the sea lamprey NCCa.…”

Tissue- and Salinity-specific Na–Cl Cotransporter (NCC) Orthologues Involved in the Sea lamprey (Petromyzon Marinus) Adaptive Osmoregulation

“…The transcription of the sea lamprey ncca in both the gills and kidney is particularly interesting because, in teleost shes, the NCC in the gills (NCC2) and kidney (NCC1) are two distinct NCC isoforms 31,34,51 . It is important to note that the elasmobranch NCC also exhibits FW-speci c function in the gills and kidney 32,53 , similar to the expression pattern of the sea lamprey NCCa.…”

Molecular and morphological investigations on the renal mechanisms enabling euryhalinity of red stingray Hemitrygon akajei

“…In euryhaline Atlantic stingrays, both the glomerular filtration rate (GFR) and urine flow rate (UFR) were markedly increased after transfer from ambient SW to 50%-diluted SW, suggesting that the kidney of stingrays vigorously excretes excess water gained from the diluted environment as in the case of FW teleost fishes ( Janech et al, 2006 ). The concomitant increases in reabsorption of NaCl and urea to produce dilute urine in the hypo-osmotic environment were also demonstrated in the Atlantic stingray ( Janech et al, 2006 ) and bull shark ( Imaseki et al, 2019 ). In bull shark, Na + -Cl - cotransporter (NCC) was suggested to be a key renal transporter facilitating the reabsorption of both NaCl and urea in the FW-acclimated bull shark ( Imaseki et al, 2019 ).…”