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Zoological Letters 2017 3 :22

https://doi.org/10.1186/s40851-017-0081-8

© The Author(s).2017

Received: 19December2016

Accepted: 11October2017

Published: 12December2017

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.

Sodium storage Osmoregulation Mucus Teleost Euryhaline Transcriptome

Studies on osmoregulation have focused on the transport of ions to drive water movement and it is generally accepted that ions in the extracellular fluid (ECF) are regulated at a relatively constant level to maintain plasma osmolality (ca. 300-350 mOsm) in most vertebrates. The gill, intestine, and kidney are the major osmoregulatory organs in teleosts and successful acclimation in both freshwater (FW) and seawater (SW) environments depends on the composition of epithelial transporters and channels, and metabolic and structural adjustments in those tissues. Externally, the teleost gill possesses various types of ionocytes that absorb ions in FW and excrete ions in SW [ Merrell J13AcXVPL
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]. Teleosts drink copiously in SW and the intestine absorbs the imbibed water by actively taking up monovalent ions (Na + /Cl ) and precipitating divalent ions (Ca 2+ , Mg 2+ , SO 4 2− ) [ 4 , Tizian Liliane 03 Women’s Bootees Grey Grey 1gCBwGxPdJ
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]. The kidneys perform glomerular filtration to excrete excess water by producing copious diluted urine in FW [ LEIT YFF Gift Women Dance Shoes Ballroom Latin Dance Tango Dancing Shoes 85cmRed41 5SrrsyxicD
, 8 ] while those in SW actively secrete divalent ions in the proximal tubules [ Keen Womens Terradora WP Hiking Shoe Silver Birch/Canteen 7 M US n6f4Lc1y9
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]. These mechanisms were mostly derived from studies using euryhaline species (e.g. eels, salmon, killifish, etc.) fully acclimated to either FW or SW, whereas knowledge during the early transition phase between salinities is limited.

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