Rapid regulation of Na+ and Cl- flux rates in killifish after acute salinity challenge

The common killifish lives in tidal marshes and estuaries where it encounters hourly fluctuations in salinity. Radiotracers (22Na, 36Cl) were employed to examine its ability to rapidly adjust unidirectional influx and efflux rates of Na+ and Cl- in the 8-h period after acute transfer from the acclimation medium (10% sea water, SW) to either 100% SW or fresh water (FW). Flux rates were measured over 0.5–1.0 h intervals, and compared with stable rates measured at 12 h–7 d post-transfer under identical conditions in an earlier study. After transfer to 100% SW, Na+ and Cl- influx rates increased 7-fold with large overshoots in the first hour, but thereafter decreased by 35–50%, reaching levels at 1–2 h not significantly different from 12 h–7 d values. Na+ and Cl- efflux rates increased by 40–100% in the first hour post-transfer but thereafter rose gradually, reaching the 12 h–7 d values only by 5.0–5.5 h for Na+, and remaining significantly lower even at 7.5–8.0 h for Cl-. After transfer to FW, Na and Cl influx rates dropped by 97–99% in the first hour. Na+ influx recovered to a level equal to about 40% of the 12 h–7 d rate by 1–2 h, thereafter not changing through 8 h. Cl- influx exhibited no recovery, and remained negligible even at 12 h–7 d. Na+ and Cl- efflux rates decreased by 26–27% in the first 0.5 h after transfer to FW, and reached levels comparable to the 12 h–7 d values by 1.0–1.5 h for Na+ and 2.5–3.0 h for Cl- Overall, there were two clear trends. The passive components (Na+ and Cl- influxes in 100% SW, Na+ and Cl- effluxes in FW) were regulated more rapidly than the active fluxes (Na+ and Cl- effluxes in 100% SW, Na+ influx in FW), and Na+ balance was regulated more quickly and precisely than Cl- balance, for transfers in both directions. Rapid adjustments of both active and passive fluxes suggest that they involve direct responses of channels and tight junctions to salinity changes, as well as post-translational mechanisms of transporter regulation. These short-term responses are effective in changing ion flux rates long before “structural” re-organizations of the gill transport machinery occur by genomic mechanisms. This strategy, combined with an ability to tolerate internal ionic disturbances, is of obvious benefit in a species which routinely encounters hourly salinity fluctuations in its natural environment.

► After salinity transfer, killifish exhibit rapid changes in Na+ and Cl- fluxes.
► Passive fluxes of both ions are regulated more rapidly than active fluxes.
► Na+ balance is regulated more quickly and precisely than Cl- balance.
► Waterborne Cl- uptake is negligible in freshwater, implicating dietary acquisition.
► Rapid flux adjustments are likely of non-genomic origin.