In Vivo Action of Ammonia on Ion Transport Function in Liver and Heart Mitochondria of Immersion-Stressed Air-Breathing Fish (Anabas testudineus Bloch)
Authors
-
Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala ,IN
Shilpa Narayan -
Inter-University Centre for Evolutionary and Integrative Biology (iCEIB), School of Life Sciences, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala ,INValsa S. Peter
-
Department of Zoology, University of Kerala, Kariavattom, Thiruvananthapuram – 695581, Kerala ,INM. C. Subhash Peter
DOI:
https://doi.org/10.18311/jer/2018/24830Keywords:
Ammonia, Anabas testudineus, Fish, Hypoxia, Ion Transport, Mitochondria, StressAbstract
Ammonia, as an endogenous respiratory gas, is produced during protein and amino acid metabolism. Accumulation of excess ammonia is toxic, and fishes have developed mechanisms to defend against ammonia toxicity. Here, we tested the in vivo action of ammonia in an air-breathing fish to find how it modulates mitochondrial ion transport in fish heart and liver. We thus analysed the activity pattern of mitochondrial ion transporters such as mitochondrial Ca2+ATPase, mitochondrial H+ATPase and mitochondrial F1F0 ATPase in heart and liver of air-breathing fish Anabas testudineus which were kept for immersion-induced hypoxia stress. In addition, plasma metabolites such as glucose and lactate were also quantified. Oral administration of ammonia solution [(NH4)2SO4; 50ng g-1] for 30 min increased mit.Ca2+ATPase activity in heart but lowered its activity in liver mitochondria. A reduced mit.H+ATPase activity was found in heart but in liver its activity showed increase after ammonia treatment. F1F0 ATPase increased significantly in heart but showed reduced activity in liver mitochondria. Administration of ammonia in immersion-stressed fish, however, nullified the excitatory response of heart and liver mitochondria in the immersion-stressed fish. Overall, the data indicate that ammonia can play a significant physiological role in the regulation of mitochondrial ion homeostasis in the liver and heart of air-breathing fish during their acclimation to hypoxia stress.
Downloads
Metrics
Downloads
Published
How to Cite
Issue
Section
References
Evans DH, Cameron JN. Gill ammonia transport. J Exp Zool. 1986; 239:17–23.
Weihrauch D, Wilkie MP, Walsh PJ. Ammonia and urea transporters in gills of fish and aquatic crustaceans. J Exp Biol. 2009; 212(11):1716–30.
Wang R. Gasotransmitters: growing pains and joys. Tr Biochem Sci. 2014; 39(5):227–32. doi:10.1016/j.tibs.2014.03.003.
Kaushik SJ, Seiliez I. Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs.Aquacult Res. 2010; 41(3):322–32. doi:10.1111/j.13652109.2009.02174.x
Smutna M, Vorlova L, Svobodova Z. Pathobiochemistry of ammonia in the internal environment of fish (Review).Acta Vet Brno. 2002; 71:169–81.
Wagner CA, Devuyst O, Belge H, Bourgeois S, Houillier P. The rhesus protein RhCG: a new perspective in ammonium transport and distal urinary acidification. Kidney Int., 2011; 79(2):154–161. doi:10.1038/ki.2010.386
Ishimatsu A. Evolution of the Cardiorespiratory System in Air-Breathing Fishes. Aqua-BioScience Monographs. 2012; Vol. 5: pp. 1–28.
Icardo JM. The teleost heart: A morphological approach. In: I Sedmera, T Wang (Eds.), Ontogeny and Phylogeny of the Vertebrate Heart. Springer. 2012; 35–53. doi:10.1007/9781-4614-3387-3_2
Aho E, Vornanen M. Ca2+-ATPase activity and Ca2+ uptake by sarcoplasmic reticulum in fish heart: effects of thermal acclimation. J Exp Biol. 1998; 201(Pt 4):525–32.
Dube PN, Alavandi S, Hosetti BB. In vivo changes in the activity of (gill, liver and muscle) ATPases from Catla catla as a response of copper cyanide intoxication. Eu J Exp Biol.2012; 2(4):1320–25.
Graham JB. Air Breathing Fishes: Evolution, Diversity and Adaptation. San Diego: Academic Press. 1997.
Wood CM. Dogmas and controversies in the handling of nitrogenous wastes: is exogenous ammonia a growth stimulant in fish? J Exp Biol. 2004; 207:2043–54.
Ip YK, Chew SF. Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol. 2010; 1:134.
Ip YK, Chew SF. Air-breathing and excretory nitrogen metabolism in fishes. Acta Histochem. 2018; 120(7): 68090. doi:10.1016/j.acthis.2018.08.013
Peter VS, Joshua EK, Wendelaar Bonga SE, Peter MCS.Metabolic and thyroidal response in air-breathing perch (Anabas testudineus) to water-borne kerosene. Gen Comp Endocrinol. 2007; 152:198–205.
Peter MCS, Leji J, Peter VS. Ambient salinity modifies the action of triiodothyronine in the air-breathing fish Anabas testudineus Bloch: effects on mitochondria-rich cell distribution, osmotic and metabolic regulations. Gen CompEndocrinol. 2011; 171:225–31.
Peter MCS, Mini VS, Bindulekha DS, Peter VS. Short-term In situ effects of prolactin and insulin on ion transport in liver and intestine of freshwater climbing perch (Anabas testudineus Bloch). J Endocrinol Reprod. 2014; 18(1):47– 58.
Alexander JB, Ingram GA. A comparison of five of the methods commonly used to measure protein concentrations in fish sera. J Fish Biol. 1980; 16:115–22.
Thillart GV, Raaji MV. Endogenous fuels; noninvasive versus invasive. In Hochachka PW, Mommsen TP (Eds)., Biochemistry and Molecular Biology of Fishes, Metabolic Biochemistry, Amsterdam: Elsevier. 1995; 4:33–63
Ballantyne JS. Amino acid metabolism. In: Wright PA, Anderson PM (Eds)., Fish Physiology, Nitrogen Excretion, New York: Academic Press. 2001; 19:77–107.
Metwally MAA, Wafeek M. Effect of ammonia toxicity on carbohydrate metabolism in Nile Tilapia (Oreochromis niloticus). World J Fish Marine Sci. 2014; 6 (3):252-61.
Bardon-Albaret A, Saillant EA. Effects of hypoxia and elevated ammonia concentration on the viability of red snapper embryos and early larvae. Aquaculture. 2016; 459:148– 55. doi:10.1016/j.aquaculture.2016.03.042
Jensen FB, Hansen MN. Differential uptake and metabolism of nitrite in normoxic and hypoxic goldfish. Aquat Toxicol. 2011; 101(2):318–25.
Walsh PJ, Wei Z, Wood CM, et al. Nitrogen metabolism and excretion in Allenbatrachus grunniens(L): effects of variable salinity, confinement, high pH and ammonia loading. J Fish Biol. 2004; 65(5):1392–411. doi:10.1111/ j.0022-1112.2004.00538.x
Finkel T, Menazza S, Holmstrom KM, et al. The ins and outs of mitochondrial calcium. Circ Res. 2015; 116(11):1810–19.
Shiels HA, Galli GLJ, Block BA. Cardiac function in an endothermic fish: cellular mechanisms for overcoming acute thermal challenges during diving. Proc Biol Sci.s 2014; 282(1800): 20141989.doi:10.1098/rspb.2014.1989
Vornanen M, Shiels HA, Farrell AP. Plasticity of excitation– contraction coupling in fish cardiac myocytes. Comp Biochem Physiolt A: Mol Integr Physiol. 2002; 132(4):827– 46.
Castilho PC, Landeira-Fernandez AM, Morrissette J, Block BA. Elevated Ca2+ ATPase (SERCA2) activity in tuna hearts: Comparative aspects of temperature dependence. Comp Biochem Physiol A Mol Integr Physiol. 2007; 148(1 SPEC.ISS.):124–32.
Duncan TM. The ATP synthase: Parts and properties of a rotary motor. The Enzymes. 2003; 203–275. doi:10.1016/ s1874-6047(04)80006-4.
Neupane P, Bhuju S, Thapa N, Bhattarai HK. ATP synthase: Structure, function and inhibition. Biomol Concepts. 2018; 10(1):1–10.
Mitome N, Ono S, Sato H, et al. Essential arginine residue of the F0-a subunit in F0F1-ATP synthase has a role to prevent the proton shortcut without c-ring rotation in the F0 proton channel. Biochem J. 2010; 430(1):171–77.
Sun Y. F1F0-ATPase functions under markedly acidic conditions in bacteria. In: Chakraborti S, Dhalla N. (Eds) Regulation of Ca2+- ATPases, V-ATPases and F-ATPases. Advances in Biochemistry in Health and Diseases. 2016; 14:459–468.
