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Zoological Lett. 2017 Dec 12;3:22. doi: 10.1186/s40851-017-0081-8. eCollection 2017.

A sodium binding system alleviates acute salt stress during seawater acclimation in eels.

Author information

1
Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa City, Japan.
2
Department of Biomolecular Science, Toho University, Funabashi City, Japan.
3
Department of Computational Biology, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa City, Japan.
4
Bioinformatics Research Unit, Advanced Center for Computing and Communication, RIKEN, Wako City, Japan.
5
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan.

Abstract

Background:

Teleosts transiting from freshwater (FW) to seawater (SW) environments face an immediate osmotic stress from ion influxes and water loss, but some euryhaline species such as eels can maintain a stable plasma osmolality during early SW exposure. The time course changes in the gene expression, protein abundance, and localization of key ion transporters suggested that the reversal of the ion transport systems was gradual, and we investigate how eels utilize a Na-binding strategy to slow down the ion invasion and complement the transporter-mediated osmoregulation.

Results:

Using an electron probe micro-analyzer, we localized bound Na in various eel tissues in response to SW transfer, suggesting that the Na-binding molecules were produced to sequester excess ionic Na+ to negate its osmotic potential, thus preventing acute cellular dehydration. Mucus cells were acutely activated in digestive tract, gill, and skin after SW transfer, producing Na-binding molecule-containing mucus layers that fence off high osmolality of SW. Using gel filtration HPLC, some molecules at 18 kDa were found to bind Na in the luminal secretion of esophagus and intestine, and higher binding was associated with SW transfer. Transcriptome and protein interaction results indicated that downregulation of Notch and β-catenin pathways, and dynamic changes in TGFβ pathways in intestine were involved during early SW transition, supporting the observed histological changes on epithelial desquamation and increased mucus production.

Conclusions:

The timing for the activation of the Na-binding mechanism to alleviate the adverse osmotic gradient was temporally complementary to the subsequent remodeling of branchial ionocytes and transporting epithelia of the digestive tract. The strategy to manipulate the osmotic potential of Na+ by specific binding molecules is similar to the osmotically inactive Na described in human skin and muscle. The Na-binding molecules provide a buffer to tolerate the salinity changes, which is advantageous to the estuary and migrating fishes. Our data pave the way to identify this unknown class of molecules and open a new area of vertebrate osmoregulation research.

KEYWORDS:

Euryhaline; Mucus; Osmoregulation; Sodium storage; Teleost; Transcriptome

Conflict of interest statement

The animal study was performed according to the Guideline for Care and Use of Animals approved by the Animal Experiment Committee of the University of Tokyo.Not applicable.The authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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