Strategies for surviving high concentrations of environmental ammonia in the swamp eel Monopterus albus.
The swamp eel Monopterus albus lives in muddy ponds, swamps, canals, and rice fields in the tropics. It encounters high concentrations of environmental ammonia (HEA) during dry seasons or during agricultural fertilization in rice fields. This study aimed at determining the tolerance of M. albus to environmental ammonia and at elucidating the strategies that it adopts to defend against ammonia toxicity in HEA. In the laboratory, M. albus exhibited very high environmental ammonia tolerance; the 48-, 72-, and 96-h median lethal concentrations of total ammonia at pH 7.0 and 28 degrees C were 209.9, 198.7, and 193.2 mM, respectively. It was apparently incapable of actively excreting ammonia against a concentration gradient. In addition, it did not detoxify ammonia to urea, the excretion of which would lead to a loss of nitrogen and carbon, during ammonia loading. The high tolerance of M. albus to HEA was attributable partially to its exceptionally high tolerance to ammonia at the cellular and subcellular levels. During the 144 h of exposure to 75 mM NH(4)Cl at pH 7.0, the ammonia contents in the muscle, liver, brain, and gut of M. albus reached 11.49, 15.18, 6.48, and 7.51 mu mol g(-1), respectively. Such a capability allowed the accumulation of high concentrations of ammonia in the plasma (3.54 mu mol mL(-1)) of M. albus exposed to HEA, which would reduce the net influx of exogenous ammonia. Subsequent to the buildup of internal ammonia levels, M. albus detoxified ammonia produced endogenously to glutamine. The glutamine contents in the muscle and liver reached 10.84 and 17.06 mu mol g(-1), respectively, after 144 h of exposure to HEA, which happened to be the highest known for fish. Unlike urea, the storage of glutamine in the muscle during ammonia loading allowed its usage for anabolic purposes when the adverse environmental condition subsides. Glutamine synthetase activity increased significantly in the liver and gut (2.8- and 1.5-fold, respectively) of specimens exposed to HEA for 144 h. These results suggest that the liver was the main site of ammonia detoxification and the gut was more than a digestive/absorptive organ in M. albus. Monopterus albus did not undergo a reduction in amino acid catabolism during the first 24 h of ammonia exposure. However, assuming a total inhibition of excretion of endogenous ammonia, there was a deficit of -312 mu mol N between the reduction in nitrogenous excretion (3,360 mu mol N) and the retention of nitrogen (3,048 mu mol N) after 72 h of aerial exposure. The deficit became much greater after 144 h, reaching a value of -3,243 mu mol N. These results suggest that endogenous ammonia production in M. albus was suppressed in order to prevent the newly established internal steady state concentration of ammonia from rising to an intolerable level after an extended period of exposure to HEA.
Ip
Yuen K
YK
Department of Biological Science, National University of Singapore, Kent Ridge, Singapore 117543, Republic of Singapore. dbsipyk@nus.edu.sg
Tay
Angeline S L
AS
Lee
Kong H
KH
Chew
Shit F
SF
D000596:Amino Acids / Q000378:metabolism; D000641:Ammonia / Q000493:pharmacokinetics / Q000633:toxicity*; D000704:Analysis of Variance; D000818:Animals; D001822:Body Burden; D004777:Environment; D005974:Glutamate-Ammonia Ligase / Q000378:metabolism; D005973:Glutamine / Q000097:blood / Q000378:metabolism; D007928:Lethal Dose 50; D008099:Liver / Q000378:metabolism; D009584:Nitrogen / Q000378:metabolism; D012846:Singapore; D023701:Smegmamorpha / Q000378:metabolism / Q000502:physiology*; D013997:Time Factors; D023382:Toxicity Tests, Acute
D000596:Amino Acids; D005973:Glutamine; D000641:Ammonia; D005974:Glutamate-Ammonia Ligase; D009584:Nitrogen