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
Log in using your username and password
Log in through your institution
Pay Per Article - You may access this article (from the computer you are currently using) for 1 day for US$30.00 .
Regain Access - You can regain access to a recent Pay per Article purchase if your access period has not yet expired.
Article navigation
Related articles
Cited by...
More in this TOC section
Similar articles
Other journals from The Company of Biologists
Editorial – The changing of the guard
In his Editorial, Hans Hoppeler announces that he will be stepping down as Editor-in-Chief of JEB in July 2020. He reflects on the history of JEB, why he has enjoyed his tenure as JEB’s Editor-in-Chief and the recent developments in the publishing world.
Editors’ choice – Parental stressor exposure simultaneously conveys both adaptive and maladaptive larval phenotypes through epigenetic inheritance in the zebrafish (Danio rerio)
An oil spill is never a good thing, but Naim Bautista and Warren Burggren have shown that zebrafish can pass on resistance to the damaging effects of an oil-spiked diet to their offspring.
The derivative of force with respect to time does not have a standard term in physics. In their new Commentary, David C. Lin and his colleagues propose that the term ‘yank’ should be used to denote the time derivative of force.
Runners waste energy every time their legs stop swinging, but now a team of scientists from the US and Canada have shown that a springy ankle tether can reduce runners’ energy costs by 6.4%, which is nearly the entire cost of swinging the limbs. Read the full research article here.
Journal of Experimental Biology is pleased to announce a new partnership with Publons! This allows reviewers to easily track and verify every review by choosing to add the review to their Publons profile when completing the review submission form. Publons also makes it simple for reviewers to showcase their peer review contributions in a format that can be included in job and funding applications (without breaking reviewer anonymity). Read the official announcement here!
The Company of Biologists provides grants to fund scientific meetings, workshops and conferences in the fields covered by our journals. Typically, meetings with fewer than 100 people may be granted up to £2,000, increasing up to £6,000 for about 400 people. The next deadline to apply is 28 November 2019.
preLights – preLights reaches 500 posts!
The success of preLights is down to the hard work of our preLighters. Head over to the preLights website to find out more about our most active early-career-researchers.