Adaptations of a deep sea scavenger: High ammonia tolerance and active NH4+ excretion by the Pacific hagfish (Eptatretus stoutii)

Abstract

The Pacific hagfish (Eptatretus stoutii) has an exceptional ability to both withstand and recover from exposure to high external ammonia (HEA). This tolerance is likely due to the feeding behavior of this scavenger, which feeds on intermittent food falls of carrion (e.g. fish, large marine mammals) during which time it may be exposed to high concentrations of total ammonia (TAmm=NH3+NH4+) while burrowed inside the decomposing carcass. Here we exposed hagfish to 20mmolL−1TAmm for periods of up to 48h and then let animals recover in ammonia-free seawater. During the 48h HEA exposure period, plasma TAmm increased 100-fold to over 5000μmolL−1 while ammonia excretion (Jamm) was transiently inhibited. This increase in plasma TAmm resulted from NH3 influx down massive inwardly directed ΔPNH3 gradients, which also led to a short-lived metabolic alkalosis. Plasma [TAmm] stabilized after 24–48h, possibly through a reduction in NH3 permeability across the body surface, which lowered NH3 influx. Ammonia balance was subsequently maintained through the re-establishment of Jamm against an inwardly directed ΔPNH3. Calculations of the Nernst potential for ammonia strongly indicated that Jamm was also taking place against a large inwardly directed NH4+ electrochemical gradient. Recovery from HEA in ammonia-free water was characterized by a large ammonia washout, and the restoration of plasma TAmm concentrations to near control concentrations. Ammonia clearance was also accompanied by a residual metabolic acidosis, which likely offset the ammonia-induced metabolic alkalosis seen in the early stages of HEA exposure. We conclude that restoration of Jamm by the Pacific hagfish during ammonia exposure likely involves secondary active transport of NH4+, possibly mediated by Na+/NH4+ (H+) exchange.