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.
FOOTNOTES
Competing interests
The authors declare no competing or financial interests.
Author contributions
Conceptualization: S.H.; Methodology: I.I., S.H.; Validation: I.I., S.H.; Formal analysis: Y. Hara, Y. Honda, S.K.; Investigation: I.I., M.W., Y. Hara, T.W., S.T., K.K., Y. Honda, K.U., K.M., R.M., Y.M., M.N., W.T., S.K., S.H.; Resources: K.U., K.M., R.M., Y.M., M.N.; Writing - original draft: I.I., S.H.; Writing - review & editing: I.I., M.W., Y. Hara, W.T., S.K., S.H.; Funding acquisition: I.I., S.H.
Funding
This study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (JSPS KAKENHI 26650110, 26291065, 17H03868) and a Research Grant from the Okinawa Churashima Foundation to S.H., and a Grant-in-Aid for JSPS Fellows (16J07895) to I.I. I.I. is supported by JSPS Research Fellowships for Young Scientists.
Data availability
The short-read data of RNA-seq analysis are available from the DNA Data Bank of Japan (DDBJ): DRX162067, DRX162068, DRX162069 and DRX162070. The partial sequences of bull shark NKAα1, NKCC2, UT and EF1α1 and houndshark EF1α1 are also available from the DDBJ: LC462277, LC462278, LC462279, LC462280 and LC462281, respectively.
Supplementary information
Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.201780.supplemental
- Received February 14, 2019.
- Accepted May 18, 2019.
- © 2019. Published by The Company of Biologists Ltd
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