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

Abstract

Sulfate (SO2−4) regulation is challenging for euryhaline species as they deal with large fluctuations of SO2−4 during migratory transitions between freshwater (FW) and seawater (SW), while maintaining a stable plasma SO2−4 concentration. Here, we investigated the regulation and potential role of sulfate transporters in Atlantic salmon during the preparative switch from SO2−4 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 SO2−4 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 SO2−4 excretion through the upregulated slc26a6a1, the most likely secretory transport candidate in fish, which together with the slc26a1a transporter likely removes excess SO2−4 , and ultimately enable the regulation of normal plasma SO2−4 levels in SW.