Sulfate homeostasis in Atlantic salmon is associated with differential regulation of salmonid-specific paralogs in gill and kidney.

Marius Takvam,Naouel Gharbi,Tom O Nilsen,Harald Kryvi,Elsa Denker

doi:10.14814/phy2.15059

Marius Takvam, Naouel Gharbi + Show 3 more

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https://doi.org/10.14814/phy2.15059

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Abstract

Sulfate (SO42‐) regulation is challenging for euryhaline species as they deal with large fluctuations of SO42‐ during migratory transitions between freshwater (FW) and seawater (SW), while maintaining a stable plasma SO42‐ concentration. Here, we investigated the regulation and potential role of sulfate transporters in Atlantic salmon during the preparative switch from SO42‐ uptake to secretion. A preparatory increase in kidney and gill sodium/potassium ATPase (Nka) enzyme activity during smolt development indicate preparative osmoregulatory changes. In contrast to gill Nka activity a transient decrease in kidney Nka after direct SW exposure was observed and may be a result of reduced glomerular filtration rates and tubular flow through the kidney. In silico analyses revealed that Atlantic salmon genome comprises a single slc13a1 gene and additional salmonid‐specific duplications of slc26a1 and slc26a6a, leading to new paralogs, namely the slc26a1a and ‐b, and slc26a6a1 and ‐a2. A kidney‐specific increase in slc26a6a1 and slc26a1a during smoltification and SW transfer, suggests an important role of these sulfate transporters in the regulatory shift from absorption to secretion in the kidney. Plasma SO42‐ in FW smolts was 0.70 mM, followed by a transient increase to 1.14 ± 0.33 mM 2 days post‐SW transfer, further decreasing to 0.69 ± 0.041 mM after 1 month in SW. Our findings support the vital role of the kidney in SO42‐ excretion through the upregulated slc26a6a1, the most likely secretory transport candidate in fish, which together with the slc26a1a transporter likely removes excess SO42‐, and ultimately enable the regulation of normal plasma SO42‐ levels in SW.

Highlights

Fish live in aquatic environments that range from hypo- osmotic to hyper-osmotic and are more vulnerable to changes in body fluids compared to terrestrial animals (Takei et al, 2014)
The ion regulatory roles of gills and intestine are well studied in euryhaline fish moving between FW and SW environments (Evans, 2010; Evans et al, 2005; Hiroi & McCormick, 2012; McCormick, Farell, et al, 2013; Grosell, 2010; Sundell & Sundh, 2012; Whittamore, 2012), while knowledge pertaining to the ion regulation mechanisms in the euryhaline teleost kidney is more limited, despite major changes in renal function are necessary when moving between FW and SW environments (Takvam et al, 2021)
Affinity measurements of different ions (SO24−/ HCO32−/Cl−) are required before firm conclusions regarding the role of Slc26a6a2 in the gills

Summary

| INTRODUCTION

Fish live in aquatic environments that range from hypo- osmotic to hyper-osmotic and are more vulnerable to changes in body fluids compared to terrestrial animals (Takei et al, 2014). SW teleosts osmotically loose water and passively gain ions from the environment (1000 mOsm/kg) (Evans, 1984; Evans et al, 2005; Marshall & Grosell, 2006) To compensate they need to drink seawater to absorb water in the intestines (Whittamore, 2012), loading the blood with NaCl that is actively secreted across gills (Evans, 2010; Hwang et al, 2011; Hiroi & McCormick, 2012; McCormick, Regis, et al, 2013; Takei et al, 2014). The purpose of this study was to 1) identify key SO24− transporters in the salmon genome and their tissue distribution and 2) determine changes in SO24− transporters expression during smoltification and SW acclimation

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| Summary and future perspective