Vigorous SO42– influxviathe gills is balanced by enhanced SO42– excretion by the kidney in eels after seawater adaptation

Abstract

SUMMARY Sulfate (SO42–) is maintained at ∼1 mmol–1 l–1 in teleost fishes that are exposed to media of varying SO42– concentrations. We first measured plasma SO42– concentration in euryhaline fishes that adapt to both SO42–-poor freshwater (<0.5 mmol l) and SO42–-enriched seawater (30 mmol l–1). Unlike Mozambique tilapia and chum salmon, Japanese eels maintained higher plasma SO42– concentration in freshwater (6.2±2.3 mmol l–1) than in seawater (0.7±0.1 mmol l–1). We then analyzed the whole-body SO42– budget using 35SO42–. 35SO42– influx in seawater-adapted eels occurred by 84.5% via body surfaces and 15.5% via digestive tracts. The SO42– influx was higher in seawater eels (1.55 μmol kg–1 h–1) than in freshwater eels (0.09 μmol kg–1 min–1), but it was facilitated in freshwater eels when the difference in SO42– concentrations between plasma and environment was taken into account (freshwater eels, 6.2 vs 0.3 mmol l–1; seawater eels, 0.7 vs 30 mmol l–1). One hour after injection of 35SO42– into the blood of seawater eels, the kidney excreted ∼97% of the ionized form, whereas the radioactivity increased gradually in the medium and the rectal fluid more than 3 h after injection. As the radioactivity was poorly adsorbed by anion-exchange resin, 35SO42– in the blood may be incorporated into cells and excreted by the intestine, gills and skin, probably as mucus. These results show that freshwater eels take up SO42– actively from the environment, but seawater eels cope with the obligatory influx of SO42– through the gills by excreting excess SO42–via the kidney and in mucus.

Ion Transporters and Osmoregulation in the Kidney of Teleost Fishes as a Function of Salinity

“…Moreover, eels seems to have much higher plasma SO 4 2− concentration in FW (Farrell and Lutz, 1975) compared to other euryhaline species examined ( Watanabe and Takei, 2012). The absorptive features of the SLC13A1 transporter in the eel might reflect such elevated plasma SO 4 2− levels, since both chum salmon (Oncorhynchus keta) and tilapia have low levels of SO 4 2− , and no SLC13A1 transporter has been identified in these species ( Watanabe and Takei, 2012). The SLC13A1 likely facilitates elevated plasma SO 4 2− levels, probably particular important for FW eels, because this species lacks active Cl − uptake at the gills (Nakada et al, 2005;Kato and Watanabe, 2016).…”

“…As pointed out by the authors, this model is partly based on the mammalian counterpart and FW eels are the only euryhaline species where the SLC13A1 has been detected in the kidney ( Kato and Watanabe, 2016). Moreover, eels seems to have much higher plasma SO 4 2− concentration in FW (Farrell and Lutz, 1975) compared to other euryhaline species examined ( Watanabe and Takei, 2012). The absorptive features of the SLC13A1 transporter in the eel might reflect such elevated plasma SO 4 2− levels, since both chum salmon (Oncorhynchus keta) and tilapia have low levels of SO 4 2− , and no SLC13A1 transporter has been identified in these species ( Watanabe and Takei, 2012).…”

“…26 mM). FW teleosts actively take up SO 4 2− from the environment, whereas in SW, there is an unavoidable influx of SO 4 2− through the gills, and perhaps slight uptake in the gut: 97% of the excess SO 4 2− is excreted through the kidney ( Watanabe and Takei, 2012).…”

The digestive tract as an essential organ for water acquisition in marine teleosts: lessons from euryhaline eels

“…As shown in Table 1 , ingested SW is processed gradually according to its passage through the digestive tract of eels [ 113 , 207 , 241 , 257 ]. Similar results have been reported in the digestive tract of the winter flounder, Pseudopleuronectes americanus [ 166 ].…”

“…As SLC26a1 exhibits high affinity for SO 4 2− , it is possible that apical SLC26a6 and basolateral SLC26a1 work in concert for transcellular secretion of HCO 3 − in exchange for SO 4 2− absorption in the SW eel intestine (see 6.2). Cooperation of the two sulfate transporters has been observed in the proximal tubules of SW eel kidneys [ 257 ]. The SLC4 family of AEs also contains candidates for HCO 3 − secretion: two AE2 genes ( slc4a2a and slc4a2b ) are expressed in the eel intestine, and slc4a2a tends to be upregulated after SW transfer (Fig.…”