Functional ureogenesis and adaptation to ammonia metabolism in Indian freshwater air-breathing catfishes

Fish Physiology and Biochemistry

Volumn 33, Issue 4, 2007, Pages 283-295

  Saha, N ^a   Ratha, B K ^b  

^a NORTH EASTERN HILL UNIVERSITY   (India)

^b BANARAS HINDU UNIVERSITY   (India)

Author keywords

Ammonia toxicity; Arginase; Carbamoyl phosphate synthetase; Clarias; Evolution; Glutamine synthetase; Heteropneustes; Urea cycle

Indexed keywords

AMMONIA; CARBAMOYL PHOSPHATE SYNTHASE; ORNITHINE; UREA;

ADAPTATION; ALKALINITY; ARTICLE; CATFISH; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; EVOLUTIONARY ADAPTATION; FRESHWATER FISH; INDIA; LIVER; NONHUMAN; PROTEIN EXPRESSION; TELEOST; TISSUE DISTRIBUTION; UREA CYCLE; WATER DEPRIVATION;

CLARIAS; CLARIAS BATRACHUS; HETEROPNEUSTES; HETEROPNEUSTES FOSSILIS; PISCES; SILURIFORMES; TELEOSTEI; VERTEBRATA;

EID: 36349030217     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10695-007-9172-3     Document Type: Article

References (95)

1. Anderson PM (1976) A glutamine- and N-acetyl-L-glutamate- dependent carbamoyl phosphate synthetase activity in the teleost Micropterus salmoides. Comp Biochem Physiol 54B:261-263
2. Anderson PM (1980) Glutamine- and N-acetyl glutamate-dependent carbamyl phosphate synthetase in elasmobranchs. Science 208:291-293
3. Anderson PM (1995a) Urea cycle in fish: Molecular and mitochondrial studies. In: Wood CM, Shuttleworth TJ (eds) Fish physiology, vol 14. Academic, New York, pp 57-83
4. Anderson PM (1995b) Molecular aspects of carbamyl phosphate synthesis. In: Walsh PJ, Wright PA (eds) Nitrogen metabolism and excretion. CRC, Boca Raton, pp 33-50
5. Anderson PM (2001) Urea and glutamine synthesis: Environmental influences on nitrogen excretion. In: Wright PA, Anderson PM (eds) Fish physiology, vol 20. Academic, New York, pp 239-277
6. Barimo JF, Steele SL, Wright PA, Walsh PJ (2004) Dogmas and controversies in the handling of nitrogenous wastes: Ureotely and ammonia tolerance in early life stages of the gulf toadfish, Opsanus beta. J Exp Biol 207:2011-2020
7. Brown GW Jr., Cohen PP (1960) Comparative biochemistry of urea synthesis-III. Activities of urea-cycle enzymes in various higher and lower vertebrates. Biochem J 75:82-91
8. Campbell JW (1991) Excretory nitrogen metabolism. In: Prosser CL (ed) Environmental and metabolic animal physiology. Wiley-Liss, New York, pp 277-324
9. Campbell JW, Anderson PM (1991) Evolution of mitochondrial enzyme systems in fish: The mitochondrial synthesis of glutamine and citrulline. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 1. Elsevier, Amsterdam, pp 43-76
10. Chadwick TD, Wright PA (1999) Nitrogen excretion and expression of urea cycle enzymes in the Atlantic cod (Gadus morhua L.): A comparison of early life stages with adults. J Exp Biol 202:2653-2662
11. Chakravorty J, Saha N, Ratha BK (1989) A unique pattern of tissue distribution and sub-cellular localization of glutamine synthetase in a freshwater air-breathing teleost, Heteropneustes fossilis (Bloch). Biochem Int 19:519-527
12. Chew SF, Wong MY, Tam WL, Ip YK (2003a) The snakehead Channa asiatica accumulates alanine during aerial exposure, but is incapable of sustaining locomotory activities on land through partial amino acid catabolism. J Exp Biol 206:693-704
13. Chew SF, Ong TF, Ho L, Tam WL, Loong AM, Hiong KC, Wong WP, Ip YK (2003b) Urea synthesis in the African lungfish Protopterus dolloi -hepatic carbamoyl phosphate synthetase III and glutamine synthetase are up-regulated by 6 days of aerial exposure. J Exp Biol 206:3615-3624
14. Cohen PP (1976) Evolutionary and comparative aspects of urea biosynthesis. In: Grisolia S, Baguena R, Mayor F (eds) The urea cycle. John Wiley and Sons, New York, pp 21-28
15. Danulat E (1995) Biochemical-physiological adaptations of teleosts to highly alkaline, saline lakes. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 5. Elsevier, Amsterdam, pp 229-249
16. Dabrowska H, Wlasow T (1986) Sublethal effect of ammonia on certain biochemical and hematological indicators in common carp. Comp Biochem Physiol 83C:179-184
17. Dêpêche J, Gilles R, Daufresne S, Chapello H (1979) Urea content and urea production via the ornithine-urea cycle pathway during the ontogenic development of two teleost fishes. Comp Biochem Physiol 63A:51-56
18. Dkhar J, Saha N, Ratha BK (1991) Ureogenesis in a freshwater teleost: An unusual sub-cellular localization of ornithine-urea cycle enzymes in the freshwater air-breathing teleost, Heteropneustes fossilis. Biochem Int 25:1061-1069
19. Frick NT, Wright PA (2002) Nitrogen metabolism and excretion in the mangrove killifish, Rivulus marmoratus. II. Significant ammonia volatilization in a teleost during air exposure. J Exp Biol 205:91-100
20. Goldstein L, Forster RP (1965) The role of uricolysis in the production of urea by fishes and other aquatic vertebrates. Comp Biochem Physiol 14:567-576
21. Goldstein L, Janssens PA, Forster RP (1967) Lungfish Neoceratodus forsteri: Activities of ornithine-urea cycle and enzymes. Science 157:316-317
22. Graham JB (1997) Metabolic adaptation. In: Graham JB, Lee JH (eds) Air-breathing fishes: Evolution, diversity and adaptation. Academic Press, San Diego, California, pp 223-240
23. Graham JB, Lee HJ (2004) Breathing air in air: In what ways might extant amphibious fish biology relates to prevailing concepts about early tetrapods, the evolution of vertebrate air-breathing, and vertebrate land transition? Physiol Biochem Zool 77:720-731
24. Griffith RW (1991) Guppies, toadfish, lungfish, coelacanths and frogs: A scenario for the evolution of urea retention in fishes. Env Biol Fish 32:199-218
25. Helbig CC, Atkinson BG (1994) 3,5,3′-triiodothyronine-induced carbamyl phosphate synthetase gene expression is stabilized in the liver of Rana catesbeiana tadpoles during heat shock. J Biol Chem 269:11743-11750
26. Hong J, Salo WL, Lusty CJ, Anderson PM (1994) Carbamyl phosphate synthetase III, an evolutionary intermediate in the transition between glutamine-dependent and ammonia-dependent carbamyl phosphate synthetase. J Mol Biol 243:131-140
27. Huggins AK, Skutsch G, Baldwin E (1969) Ornithine-urea cycle enzymes in teleostean fish. Comp Biochem Physiol 28:587-602
28. Ip YK, Chew SF, Randall DJ (2001a) Ammonia toxicity, tolerance and excretion. In: Wright PA, Anderson PM (eds) Fish physiology, vol 20. Academic, New York, pp 109-148
29. Ip YK, Chew SF, Leong IAW, Jin Y, Lim CB, Wu RSS (2001b) The sleeper Bostrichthys sinensis (Family Eleotridae) stores glutamine and reduces ammonia production during aerial exposure. J Comp Physiol 171B:357-367
30. Ip YK, Lim CB, Chew SF, Wilson JM, Randall DJ (2001c) Partial amino acid catabolism leading to the formation of alanine in Periophthalmodon schlosseri (mudskipper): A strategy that facilitates the use of amino acids as an energy source during locomotory activity on land. J Exp Biol 204:1615-1624
31. Ip YK, Tay ASL, Lee KH, Chew SF (2004a) Strategies for surviving high concentrations of environmental ammonia in the swamp eel Monopterus albus. Physiol Biochem Zool 77:390-405
32. Ip YK, Zubaidah RM, Liew PC, Loong AM, Hiong KC, Wong WP, Chew SF (2004b) African sharptooth catfish Clarias gariepinus does not detoxify ammonia to urea or amino acids but actively excretes ammonia during exposure to environmental ammonia. Physiol Biochem Zool 77:242-254
33. Iwata K (1988) Nitrogen metabolism in the mudskipper, Periophthalmus cantonensis: Changes in free amino acids and related compounds in various tissues under conditions of ammonia loading with special reference to its high ammonia tolerance. Comp Biochem Physiol 91A:499-508
34. Iwata K, Kajimura M, Sakamoto T (2000) Functional ureogenesis in the Gobiid fish, Mugilobius abei. J Exp Biol 203:3703-3715
35. Janssens PA, Cohen PP (1966) Ornithine-urea cycle enzymes in the African lungfish Protopterus aethiopicus. Science 152:358-359
36. Jenkinson CP, Grody WW, Cederbaum SD (1996) Comparative properties of arginases. Comp Biochem Physiol 114B:107-132
37. Jhingran VG (1983) Fish and fisheries of India, 2nd edn. Hindustan Publishing Co., New Delhi
38. Jones ME (1980) Pyrimidine nucleotide biosynthesis in animals: Genes, enzymes, and regulation of UMP biosynthesis. Ann Rev Biochem 49:253-280
39. Jow LY, Chew SF, Lim CB, Anderson PM, Ip YK (1999) The marble goby Oxyeleotris marmoratus activates hepatic glutamine synthetase and detoxifies ammonia to glutamine during air exposure. J Exp Biol 202:237-245
40. Kharbuli ZY, Datta S, Biswas K, Sarma D, Saha N (2006) Expression of ornithine-urea cycle enzymes in early life stages of air-breathing walking catfish Clarias batrachus and induction of ureogenesis under hyper-ammonia stress. Comp Biochem Physiol 143B:44-53
41. Korte JJ, Salo WL, Cabrera VM, Wright PA, Felskie AK, Anderson PM (1997) Expression of carbamyl phosphate synthetase III mRNA during the early stages of development and in muscle of adult rainbow trout (Oncorhynchus mykiss). J Biol Chem 272:6270-6277
42. Krebs HA, Henseleit K (1932) Studies on urea formation in animal organism. Hoppe-Sylers Z Physiol Chem 210:33-66
43. Lindley TE, Scheiderer CL, Walsh PJ, Wood CM, Bergman HL, Bergman AL, Laurent P, Wilson P, Anderson PM (1999) Muscle as the primary site of urea cycle enzyme activity in an alkaline lake-adapted tilapia, Oreochromisalcalicus grahami. J Biol Chem 274:29858-29861
44. Long JA, Gordon MS (2004) The greatest step in vertebrate history: A paleobiological review of the fish-tetrapod transition. Physiol Biochem Zool 77:700-719
45. Loong AM, Hiong KC, Lee SM, Wong WP, Chew SF, Ip YK (2005) Ornithine-urea cycle and urea synthesis in African lungfishes, Protopterus aethiopicus and Protopterus annectens, exposed to terrestrial conditions for six days. J Exp Zool 303A:354-365
46. Meijer AJ, Lamers WH, Chamuleau RAFM (1990) Nitrogen metabolism and ornithine cycle function. Physiol Rev 70:701-748
47. Mommsen TP, Walsh PJ (1989) Evolution of urea synthesis in vertebrates: the piscine connection. Science 243:72-75
48. Mommsen TP, Walsh PJ (1991) Urea synthesis in fishes: Evolutionary and biochemical perspectives. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes, vol 1. Elsevier, Amsterdam, pp 137-163
49. Munshi JSD, Hughes GM (1992) Air-breathing fishes: Their structure and life history. Oxford Publication and IBH, New Delhi
50. Pang PKT, Griffith RW, Atz JW (1977) Osmoregulation in elasmobranchs. Amer Zool 17:365-377
51. Paulus H (1983) The evolutionary history of the ornithine cycle as a determinant of its structure and regulation. Curr Top Cell Regul 22:177-200
52. 3 concentrations of 446 and 36 μM, respectively. Fish Physiol Biochem 19:59-69
53. Randall DJ, Wood CM, Perry SF, Bergman H, Maloiy GMO, Mommsen TP, Wright PA (1989) Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337:165-166
54. + against a concentration gradient. Am J Physiol 46:R1562-R1567
55. Ratha BK, Saha N, Rana RK, Choudhury B (1995) Evolutionary significance of metabolic detoxification of ammonia to urea in an ammoniotelic freshwater teleost, Heteropneustes fossilis during temporary water deprivation. Evol Biol 8&9:107-117
56. Rao GR, Tripathi SD, Sahu AK (1994) Breeding and seed production of the Asian catfish Clarias batrachus (Linnaeus). In: Manual Series, vol 3. Central Institute of Freshwater Aquaculture, Bhubaneswar, India, pp 1-47
57. Read LJ (1971) The presence of high ornithine-urea cycle enzymes activity in the teleost Opsanus tau. Comp Biochem Physiol 39B:409-419
58. Rozemeijer MJC, Plaut I (1993) Regulation of nitrogen excretion of the amphibious blenniidae Alticus kirki (Guenther, 1868) during emersion and immersion. Comp Biochem Physiol 104A:57-62
59. Saha N, Ratha BK (1986) Effect of ammonia stress on ureogenesis in a freshwater air-breathing teleost, Heteropneustes fossilis. Contemp Themes Biochem 6:342-343
60. Saha N, Ratha BK (1987) Active ureogenesis in a freshwater air-breathing teleost, Heteropneustes fossilis. J Exp Zool 241:137-141
61. Saha N, Ratha BK (1989) Comparative study of ureogenesis in freshwater, air-breathing teleosts. J Exp Zool 252:1-8
62. Saha N, Ratha BK (1990) Alterations in excretion pattern of ammonia and urea in a freshwater air-breathing teleost, Heteropneustes fossilis (Bloch) during hyper-ammonia stress. Indian J Exp Biol 28:597-599
63. Saha N, Ratha BK (1994) Induction of ornithine-urea cycle in a freshwater teleost, Heteropneustes fossilis, exposed to high concentrations of ammonium chloride. Comp Biochem Physiol 108B:315-325
64. Saha N, Ratha BK (1998) Ureogenesis in Indian air-breathing teleosts: adaptation to environmental constraints. Comp Biochem Physiol 120A:195-208
65. Saha N, Das L (1999) Stimulation of ureogenesis in the perfused liver of an Indian air-breathing catfish, Clarias batrachus, infused with different concentrations of ammonium chloride. Fish Physiol Biochem 21:303-311
66. Saha N, Chakravory C, Ratha BK (1988) Diurnal variation in renal and extra-renal excretion of ammonia-N and urea-N in a freshwater air-breathing teleost, Heteropneustes fossilis (Bloch). Proc Indian Acad Sci (Anim Sci) 97:529-537
67. Saha N, Dkhar J, Ratha BK (1995) Induction of ureogenesis in perfused liver of a freshwater teleost, Heteropneustes fossilis, infused with different concentrations of ammonium chloride. Comp Biochem Physiol 112B:733-741
68. Saha N, Dkhar J, Anderson PM, Ratha BK (1997) Carbamyl phosphate synthetases in an air-breathing teleost, Heteropneustes fossilis. Comp Biochem Physiol 116B:57-63
69. Saha N, Das L, Dutta S (1999) Types of carbamyl phosphate synthetases and subcellular localization of urea cycle and related enzymes in air-breathing walking catfish, Clarias batrachus. J Exp Zool 283:121-130
70. Saha N, Dutta S, Häussinger D (2000) Changes in free amino acid synthesis in the perfused liver of an air-breathing catfish, Clarias batrachus infused with ammonium chloride: A strategy to adapt under hyperammonia stress. J Exp Zool 286:13-23
71. Saha N, Das L, Dutta S, Goswami UC (2001) Role of ureogenesis in the mud-dwelled singhi catfish (Heteropneustes fossilis) under condition of water shortage. Comp Biochem Physiol 128B:137-146
72. Saha N, Dutta S, Bhattacharjee A (2002a) Role of amino acid metabolism in an air-breathing catfish, Clarias batrachus in response to exposure to a high concentration of exogenous ammonia. Comp Biochem Physiol 133B:235-250
73. Saha N, Kharbuli ZY, Bhattacharjee A, Goswami C, Häussinger D (2002b) Effect of alkalinity (pH 10) on ureogenesis in the air-breathing walking catfish, Clarias batrachus. Comp Biochem Physiol 132A:353-364
74. Saha N, Datta S, Biswas K, Kharbuli ZY (2003) Role of ureogenesis in tackling problems of ammonia toxicity during exposure to higher ambient ammonia in the air-breathing walking catfish Clarias batrachus. J Bioscience 28:733-742
75. Saha N, Datta S, Kharbuli ZY, Biswas K, Bhattacharjee A (2007) Air-breathing catfish, Clarias batrachus upregulates glutamine synthetase and carbamyl phosphate synthetase III during exposure to high external ammonia. Comp Biochem Physiol 147B:520-530
76. Sayer MDJ, Davenport J (1991) Amphibious fish: Why do they leave water? Rev Fish Biol Fish 1:159-181
77. Smith HW (1929) The excretion of ammonia and urea by the gills of fish. J Biol Chem 82:727-742
78. Tay ASL, Chew SF, Ip YK (2003) The swamp eel Monopterus albus reduces endogenous ammonia production and detoxifies ammonia to glutamine during 144 h of aerial exposure. J Exp Biol 206:2473-2486
79. Terjesen BF, Rønnestad I, Norberg B, Anderson PM (2000) Detection and basic properties of carbamyl phosphate synthetase III during teleosts ontogeny: A case study in the Atlantic halibut (Hippglossus hippoglossus L.). Comp Biochem Physiol 126B:521-535
80. Terjesen BF, Chadwick TD, Verreth JAJ, Rønnestad I, Wright PA (2001) Pathways of urea production during early life of an air-breathing teleost, the African catfish, Clarias gariepinus (Burchell 1822). J Exp Biol 204:2155-2165
81. 3 volatilization from alkaline regions of the body surface during ammonia loading and exposure to air in the weather loach Misgurnus anguillicaudatus. J Exp Biol 205:651-659
82. Tsui TKN, Randall DJ, Hanson J, Farrel AP, Chew SF, Ip YK (2004) Dogmas and controversies in the handling of nitrogenous wastes: Ammonia tolerance in the oriental weatherloach Misgurnus anguillicaudatus. J Exp Biol 207:1977-1983
83. Walsh PJ (1997) Evolution and regulation of urea cycle synthesis and ureotely in (Batrachoid) fishes. Annu Rev Physiol 59:299-323
84. Walsh PJ (1998) Nitrogen excretion and metabolism. In: Evans DH (ed) The physiology of fishes, 2nd edn. CRC, Boca Raton, pp 199-214
85. Walsh JP, Danulat E, Mommsen TP (1990) Variation in urea excretion in the gulf toadfish Opsanus beta. Mar Biol 106:323-328
86. Walsh PJ, Tucker BC, Hopkins TE (1994) Effects of confinement and crowding on ureogenesis in the gulf toadfish Opsanus beta. J Exp Biol 191:195-206
87. Walsh PJ, Milligan CL (1995) Effects of feeding and confinement on nitrogen metabolism and excretion in the gulf toadfish Opsanus beta. J Exp Biol 198:1559-1566
88. Walsh PJ, Mommsen TP (2001) Evolutionary considerations of nitrogen metabolism and excretion. In: Wright PA, Anderson PM (eds) Fish physiology, vol 20. Academic, New York, pp 1-30
89. Wilkie MP (1997) Mechanism of ammonia excretion across fish gills. Comp Biochem Physiol 118A:39-50
90. Wilkie MP, Wood CM (1996) The adaptations of fish to extremely alkaline environments. Comp Biochem Physiol 113B:665-673
91. Wood CM (1993) Ammonia and urea metabolism and excretion. In: Evans DH (ed) The physiology of fishes. CRC, Boca Raton, pp 379-425
92. Wright PA (1993) Nitrogen excretion and enzyme pathways for ureogenesis in freshwater tilapia (Oreochromis niloticus). Physiol Zool 66:881-901
93. Wright PA (1995) Nitrogen excretion: Three end products, many physiological roles. J Exp Biol 198:273-281
94. Wright PA, Fyhn HJ (2001) Ontogeny of nitrogen metabolism and excretion. In: Wright PA, Anderson PM (eds) Fish physiology, vol 20. Academic, New York, pp 149-200
95. Wright PA, Felskie A, Anderson PM (1995) Induction of ornithine-urea cycle enzymes and nitrogen metabolism and excretion in rainbow trout (Oncorhynchus mykiss) during early life stages. J Exp Biol 198:127-135