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Nitrogen Metabolism in the African Lungfish

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Nitrogen Metabolism in the African Lungfish View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by ScholarBank@NUS NITROGEN METABOLISM IN THE AFRICAN LUNGFISH, PROTOPTERUS ANNECTENS DURING AESTIVATION: AIR VERSUS MUD, AND NORMOXIA VERSUS HYPOXIA Loong Ai May (B.Sc. (Hons.), NUS) A THESIS SUMITTED FOR THE DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES NATIONAL UNIVERSITY OF SINGAPORE 2009 i ACKNOWLEDGEMENTS My success, my achievements, my honours, if I ever have now or future, are all yours, Prof Ip. A mere thank you is not good enough for what you have done for me. To show my gratitude to you, I will carry on thinking, practising, reflecting, and learning what you taught. Zillion thanks to Mdm for your kindness and patience to me all these years. You are a great friend and advisor, and my brain un-blocker at times, really. Billion thanks to all my friends. Your presence put a smile on my face. i TABLE OF CONTENTS ACKNOWLEDGEMENTS ......................................................................................... i TABLE OF CONTENTS ............................................................................................ ii SUMMARY ................................................................................................................. ix LIST OF TABLES ...................................................................................................... x LIST OF FIGURES ..................................................................................................... xiii 1. Abstract .................................................................................................................. 1 2. Overall Introduction ................................................................................................ 3 2.1. Aestivation involves fasting, desiccation, high temperature and corporal torpor ............................................................................................................ 3 2.2. Corporal torpor with or without metabolic depression ................................. 3 2.3. Current issues on excretory nitrogen metabolism and related phenomena in aestivators ..................................................................................................... 5 2.3.1. Aestivation in normoxia or hypoxia? ............................................... 5 2.3.2. Induction, maintenance and/or arousal? ........................................... 6 2.3.3. Preservation of biological structures or conservation of metabolic fuel? ................................................................................................. 6 2.3.4. Modifications of structures/functions or static preservation of structures? ........................................................................................ 7 2.3.5. Increased detoxification of ammonia or decreased ammonia production? ...................................................................................... 8 2.3.6. Nitrogenous wastes for excretion or nitrogenous products with specific functions? ........................................................................... 8 2.4. The present study .......................................................................................... 10 2.4.1. Excretory nitrogen metabolism in African lungfishes ..................... 10 3. Literature Review .................................................................................................... 13 3.1. Production and excretion of ammonia in fish ............................................... 13 3.1.1. Excess dietary protein and gluconeogenesis ..................................... 13 3.1.2. Ammonia production and related excretory products ....................... 15 + 3.1.3. Passage of NH3 and NH4 through biomembranes ............................ 18 3.1.4. Excretion of ammonia in ammonotelic fishes ................................... 20 3.2. Impediment of ammonia excretion and mechanisms of ammonia toxicity in fish ................................................................................................................ 22 3.2.1. Environmental conditions that impede ammonia excretion or lead to an influx of ammonia ........................................................................ 22 3.3.2. Deleterious effects of endogenous ammonia ..................................... 23 3.2.3. Deleterious effects of environmental ammonia ................................. 25 3.3. Defense against ammonia toxicity in fish ..................................................... 26 + 3.3.1. Active transport of NH4 .................................................................... 26 3.3.2. Lowering of environmental pH ......................................................... 28 3.3.3. Low NH3 permeability of cutaneous surfaces ................................... 30 3.3.4. Volatilization of NH3 ......................................................................... 31 3.3.5. Detoxification of ammonia to glutamine ........................................... 32 3.3.6. Detoxification of ammonia to urea .................................................... 35 3.3.7. High tissue ammonia tolerance, especially in the brain .................... 39 3.4. Lungfishes, with emphases on African species ............................................ 43 3.4.1. Six species of extant lungfishes belonging to three Families ............. 43 3.4.2. Only African lungfishes can aestivate in arid conditions at high temperature ......................................................................................... 44 3.4.3. Urea synthesis and CPS in African lungfishes .................................. 45 ii 3.4.4. Excretory nitrogen metabolism in the African lungfishes ................. 46 3.4.4.1. Aerial exposure ................................................................. 46 3.4.4.2. Aestivation ........................................................................ 48 3.4.4.3. Exposure to environmental ammonia ............................... 49 3.4.4.4. Feeding versus injection of NH4Cl and/or urea ................ 50 4. Chapter 1: Ornithine-urea cycle and urea synthesis in the African lungfish, Protopterus annectens, exposed to terrestrial conditions for 6 days .... 54 4.1. Introduction ................................................................................................... 55 4.2. Materials and methods .................................................................................. 58 4.2.1. Animals ............................................................................................. 58 4.2.2. Verification of the presence of OUC enzymes and GS ..................... 58 4.2.3. Evaluation of the effects of 6 days aerial exposure on nitrogenous excretion and accumulation .............................................................. 60 4.2.4. Elucidation of whether the OUC capacity would be enhanced by aerial exposure .................................................................................. 62 4.2.5. Statistical analyses ............................................................................. 62 4.3. Results ........................................................................................................... 63 4.3.1. Types of CPS ..................................................................................... 63 4.3.2. Compartmentalization of CPS and arginase ...................................... 63 4.3.3. Effects of 6 days of aerial exposure without aestivation on nitrogen metabolism in P. annectens .............................................................. 63 4.4. Discussion ..................................................................................................... 70 4.4.1. Presence of CPS III, not CPS I, in P. annectens ............................... 70 4.4.2. Aerial exposure led to suppression in ammonia production in P. annectens .......................................................................................... 71 4.4.3. Aerial exposure led to increases in rates of urea synthesis in P. annectens .......................................................................................... 73 4.4.4. A comparative perspective ................................................................ 74 4.5. Summary ........................................................................................................ 75 5. Chapter 2: Increased urea synthesis and/or suppressed ammonia production in the African lungfish, Protopterus annectens, during aestivation in air or in mud ........................................................................................................ 76 5.1. Introduction .................................................................................................... 77 5.2. Materials and methods .................................................................................. 80 5.2.1. Animals ............................................................................................. 80 5.2.2. Exposure of fish to experimental conditions and collection of samples .............................................................................................. 80 5.2.3. Determination of ammonia, urea and free amino acids (FAAs) ........ 82 5.2.4. Determination of activities of hepatic OUC enzymes ....................... 82 5.2.5. Determination of blood pO2 and muscle ATP content ...................... 83 5.2.6. Statistical analyses ............................................................................. 83 5.3. Results ..........................................................................................................
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