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Blood Lipids in Antarctic and in Temperate-Water Fish Species

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Blood Lipids in Antarctic and in Temperate-Water Fish Species J Membrane Biol (2009) 230:125–131 DOI 10.1007/s00232-009-9192-2 Blood Lipids in Antarctic and in Temperate-Water Fish Species Carlo Alberto Palmerini Æ Michela Mazzoni Æ Giancarlo Giovinazzo Æ Giuseppe Arienti Received: 26 January 2009 / Accepted: 28 July 2009 / Published online: 21 August 2009 Ó Springer Science+Business Media, LLC 2009 Abstract Antarctic fish live in very cold water and have inferred from the fluorescence anisotropy of DPH indicated adapted to this exceptional environment. Hemoglobin is that the membranes from Antarctic fish were more fluid at absent or very low; yet these fish still have erythrocytes, and any measured temperature than those obtained from fish from these we prepared ghost-like membranes. We studied living in temperate waters. The ability to live in a very cold for the first time the lipid composition of ghost membranes environment has therefore been achieved by the two Ant- and of plasma in Antarctic fish (C. hamatus and T. ber- arctic species tested in this paper by different strategies, but nacchii) and compared our results with those obtained for with the same results on fluidity. temperate-water fish (C. auratus and A. anguilla taken from Lake Trasimeno, Perugia, Italy). The membranes of Ant- Keywords Antarctic fish Á Cholesterol Á arctic fish were richer in glycerophospholipid (especially Glycerophospholipid Á Fatty acid Á Membrane fluidity phosphatidylethanolamine), whereas the membranes of temperate-water fish were richer in sphingomyelin. Unsat- urated fatty acids were particularly abundant in Antarctic The Antarctic Sea habitat (southern Ross Sea) is charac- fish: C. hamatus had long-chain unsaturated fatty acid terized by a very cold and constant temperature (-1.87°C), (especially C22:6 x-3), whereas T. bernacchii had shorter as the result of the equilibrium between ice and seawater. unsaturated fatty acyl chains (c16:1, x-7). On the other Nototheniidae are the chief fish in the Antarctic Sea and are hand, C. auratus and A. anguilla were particularly rich in characterized by an extreme stenothermy; they die if the C16:0, which constituted more than one-half of the total water temperature exceeds 4°C (Somero and DeVries fatty acid. Plasma lipids (both phospholipid and cholesterol) 1967). The ecological adaptations of Antarctic fish are were much more abundant in temperate-water fish. The important for understanding complex ecosystems such as differences in phospholipid content were mainly due to those present at low latitudes. Chionodraco hamatus and choline glycerolipids. Measures of membrane fluidity Trematomus bernacchii (Hureau et al. 1977) belong to the same suborder (Notothenioidei) and represent the highest specialization to cold adaptation (Eastman and Eakiun 2000). C. A. Palmerini Á M. Mazzoni Á G. Arienti The solubility of oxygen in seawater is inversely pro- Laboratory of Biochemistry, Department of Internal Medicine, portional to the temperature and therefore the concentration University of Perugia, Via del Giochetto, 06122 Perugia, Italy of oxygen in the Antarctic Sea is high. Moreover, the metabolic demand of fish living at cold temperatures is low G. Giovinazzo Department of Cellular and Environmental Biology, (Sidell and O’Brien 2006). These facts may decrease the University of Perugia, Via Elce di Sotto, 06120 Perugia, Italy importance of hemoglobin in Antarctic fish, which have less hemoglobin than fish living in warmer waters. In & C. A. Palmerini ( ) particular, C. hamatus (family Channichthyidae) is devoid Dipartimento di Medicina Interna, Universita` di Perugia, Via del Giochetto, 06100 Perugia, Italy of hemoglobin. The blood of this fish is white, whereas the e-mail: [email protected] blood of T. bernacchii (family Nototheniidae) is red, even 123 126 C. A. Palmerini et al.: Blood Lipids in Antarctic and in Temperate-Water Fish Species though its hemoglobin content is low compared to that Collected membranes were suspended in 1 ml of 0.32 M found in fish living in warmer waters (Ruud 1954). sucrose ? 2 mM Hepes, pH 7. Lipids, especially phospholipid, are very important for determining membrane properties, such as fluidity (Shini- Fluorescence Anisotropy Determination tzky 1984a). Therefore, it is reasonable that fish living in very cold waters may have a different lipid pattern from DPH (1,6-diphenyl–1,3,5-hexatriene; Sigma Chemical those living in temperate waters. The most consistent Company) was dissolved in tetrahydrofuran to have a 2 mM biochemical response of poikilothermic organisms to a solution that was added to ghost-like preparations. The cold environment is an increase in fatty acid unsaturation molar ratio between phospholipid and the probe was of both membrane and depot lipids (Cossins 1977a, b; B200:1. Samples were kept in the dark for 2 h before use. Hazel 1990; Hazel and Williams 1990; Logue et al. 2000). They were then poured in a cuvette already containing The composition of membrane lipid may be affected both 0.32 M sucrose ? 2 mM Hepes adjusted to pH 7 with HCl. by adaptive mechanisms in the long or the short term and Fluorescence was measured with a Shimadzu F5000 spec- by genetic differences among various species. The lipid trophotofluorimeter equipped with a polarizer (Shimadzu). composition of red blood cell membranes (ghost-like Measurements were performed at 365 nm (excitation) and membranes) of the hemoglobinless teleost, C. hamatus, and at 430 nm (emission). Temperature was varied from 4°Cto that of the red-blooded member of the same Antarctic 40°C with a thermostatic apparatus. The actual temperature suborder (T. bernacchii) were studied for the first time and was assessed through a probe inserted in the sample with an were compared with A. anguilla and C. auratus, teleosts of accuracy of ±0.1°C. Fluorescence anisotropy was calcu- temperate zones. On the other hand, plasma lipid may be lated by the equation of Shinitzky and Barenholz (1978). important to determine the overall blood viscosity in C. hamatus, which is devoid of hemoglobin. For this Lipid Extraction reason, we also investigated the plasma lipid composition. Lipids were extracted following published procedures (Folch et al. 1957): samples (corresponding to 1 ml of Materials and Methods blood) were mixed with 20 vol of chloroform:methanol (2:1, v/v) ? 4 vol of 0.9% (w/v) NaCl. The chloroformic Collection of Fish Blood phase was collected by centrifugation at 2,000 g for 5 min and washed two times with 4 vol of methanol:water (1:1, v/ Antarctic fish (Chionodraco hamatus, Trematomus ber- vol) each time. The upper phases were discarded, whereas nacchii) blood was obtained from the Italian Antarctic base the organic phase was reduced in volume under a gentle N2 (Terranova Bay, southern Sea of Ross). Blood samples flux, and the extract was dissolved in 150 ll of chloroform were centrifuged (800g 9 10 min) to separate cells from and used for further analyses. plasma, frozen at -80°C, and shipped to our laboratory. Lake Trasimeno (Italy) fish (Anguilla anguilla, Carassius Fatty Acid Methylation auratus) blood was taken during the month of July, cen- trifuged (800g 9 10 min) to separate red cells from The lipid extract (150 ll) was dried under a gentle nitrogen plasma. Red blood cells and plasma were immediately flux, mixed with 2 ml of 3% H2SO4 (w/v) in methanol, and frozen at -80°C. kept at 80°C for 1 h. A few milligrams of BHT (2,6-D-tert- butyl-4-methylphenol) was added to prevent unwanted Preparation of Ghost-Like Membranes oxidation. The reaction was stopped by placing the samples in a melting ice bath and by adding 100 ll of water to each Erythrocyte membranes were prepared as described (Steck sample. The methylated fatty acids formed in the reaction and Kant 1974): cells (corresponding to 1 ml of blood) were extracted with 5 ml of n-hexane. Samples were then were mixed (1:200, v/v) with 5 mM phosphate buffer (pH centrifuged at 1,000 g for 10 min, dried, dissolved in 30 ll 8.0) also containing 2% (w/v) EDTA. Red blood cell ghost- of n-hexane, and used for gas-chromatographic analysis. like particles were collected by centrifugation (300g 9 10 min). They were then washed with 20 ml of 8 mM Gas-Chromatographic Analysis phosphate buffer (pH 8) also containing 150 mM NaCl. Ghosts were recovered by centrifugation at 3500g for Samples were analyzed with a Carlo Erba (Milan, Italy) gas 10 min. The washing procedure was repeated twice. The chromatograph (HRG 5300 Mega Series) equipped with a pellet was suspended in 40 ml of 5 mM phosphate buffer 30-m-long (0.53-mm-internal diameter) capillary column (pH 8) and was centrifuged at 35,000g for 10 min. (Supelco; Sigma-Aldrich, Milan, Italy). The stationary 123 C. A. Palmerini et al.: Blood Lipids in Antarctic and in Temperate-Water Fish Species 127 phase was poly-alkylene glycol (PAG). The carrier gas was Cholesterol concentration was determined with cholesterol He (1 ml/min). Samples (1 ll) were then injected. The pure reference standards. injector temperature was 230°C and that of the detector was 250°C. The temperature gradient was started at 150°C and Determination of Lipid Phosphorus increased up to 190°C in 40 min. Eluted fatty acids were identified with pure reference Lipid phosphorus was determined as described by Bartlett standards and results are expressed as the percentage of (1959): briefly, dried lipid extracts were digested for 1 h each fatty acid/total fatty acid. with 0.7 ml of 70% (w/v) perchloric acid at 180°C, and phosphorus determined as described (Fiske and Subbarow Phospholipid Separation and Analysis 1929). Lipid extract aliquots were chromatographed on TLC plates Protein Determination (TLC aluminum sheets, Silica Gel 60, 20 9 20 cm; Merck, Darmstadt, Germany).
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