RT Journal Article
SR Electronic
T1 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
JF The Journal of Experimental Biology
JO J. Exp. Biol.
FD The Company of Biologists Ltd
SP jeb201780
DO 10.1242/jeb.201780
VO 222
IS 12
A1 Imaseki, Itaru
A1 Wakabayashi, Midori
A1 Hara, Yuichiro
A1 Watanabe, Taro
A1 Takabe, Souichirou
A1 Kakumura, Keigo
A1 Honda, Yuki
A1 Ueda, Keiichi
A1 Murakumo, Kiyomi
A1 Matsumoto, Rui
A1 Matsumoto, Yosuke
A1 Nakamura, Masaru
A1 Takagi, Wataru
A1 Kuraku, Shigehiro
A1 Hyodo, Susumu
YR 2019
UL http://jeb.biologists.org/content/222/12/jeb201780.abstract
AB 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.