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Research Article
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
Itaru Imaseki, Midori Wakabayashi, Yuichiro Hara, Taro Watanabe, Souichirou Takabe, Keigo Kakumura, Yuki Honda, Keiichi Ueda, Kiyomi Murakumo, Rui Matsumoto, Yosuke Matsumoto, Masaru Nakamura, Wataru Takagi, Shigehiro Kuraku, Susumu Hyodo
Journal of Experimental Biology 2019 222: jeb201780 doi: 10.1242/jeb.201780 Published 27 June 2019
Itaru Imaseki
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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  • ORCID record for Itaru Imaseki
  • For correspondence: itaru.imaseki@aori.u-tokyo.ac.jp
Midori Wakabayashi
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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  • ORCID record for Midori Wakabayashi
Yuichiro Hara
RIKEN Center for Biosystems Dynamics Research, Kobe, Hyogo 650-0047, Japan
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Taro Watanabe
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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Souichirou Takabe
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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Keigo Kakumura
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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Yuki Honda
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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Keiichi Ueda
Okinawa Churaumi Aquarium, Motobu, Okinawa 905-0206, Japan
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Kiyomi Murakumo
Okinawa Churaumi Aquarium, Motobu, Okinawa 905-0206, Japan
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Rui Matsumoto
Okinawa Churaumi Aquarium, Motobu, Okinawa 905-0206, Japan
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Yosuke Matsumoto
Okinawa Churaumi Aquarium, Motobu, Okinawa 905-0206, Japan
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Masaru Nakamura
Okinawa Churashima Foundation, Motobu, Okinawa 905-0206, Japan
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Wataru Takagi
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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Shigehiro Kuraku
RIKEN Center for Biosystems Dynamics Research, Kobe, Hyogo 650-0047, Japan
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Susumu Hyodo
Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan
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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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Keywords

  • Kidney
  • Ion transporters
  • Euryhalinity
  • Osmoregulation
  • Freshwater adaptation
  • Cartilaginous fish

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Research Article
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
Itaru Imaseki, Midori Wakabayashi, Yuichiro Hara, Taro Watanabe, Souichirou Takabe, Keigo Kakumura, Yuki Honda, Keiichi Ueda, Kiyomi Murakumo, Rui Matsumoto, Yosuke Matsumoto, Masaru Nakamura, Wataru Takagi, Shigehiro Kuraku, Susumu Hyodo
Journal of Experimental Biology 2019 222: jeb201780 doi: 10.1242/jeb.201780 Published 27 June 2019
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Research Article
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
Itaru Imaseki, Midori Wakabayashi, Yuichiro Hara, Taro Watanabe, Souichirou Takabe, Keigo Kakumura, Yuki Honda, Keiichi Ueda, Kiyomi Murakumo, Rui Matsumoto, Yosuke Matsumoto, Masaru Nakamura, Wataru Takagi, Shigehiro Kuraku, Susumu Hyodo
Journal of Experimental Biology 2019 222: jeb201780 doi: 10.1242/jeb.201780 Published 27 June 2019

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