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Hemoglobin System of Sparus Aurata: Changes in Fishes Farmed Under Extreme Conditions

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Hemoglobin System of Sparus Aurata: Changes in Fishes Farmed Under Extreme Conditions SCIENCE OF THE TOTAL ENVIRONMENT 403 (2008) 148– 153 available at www.sciencedirect.com www.elsevier.com/locate/scitotenv Hemoglobin system of Sparus aurata: Changes in fishes farmed under extreme conditions Salvatore Campoa, Giancarlo Nastasia, Angela D'Ascolaa, Giuseppe M. Campoa, Angela Avenosoa, Paola Trainaa, Alberto Calatronia, Emanuele Burrascanob, Alida Ferlazzob, Giulio Lupidic, Rosita Gabbianellic, Giancarlo Falcionic,⁎ aDepartment of Biochemical, Physiological and Nutritional Sciences, School of Medicine, University of Messina, Policlinico Universitario, Torre Biologica, 5° piano, Via C. Valeria, 98125 Messina, Italy bDepartment of Morphology, Biochemistry, Physiology and Animal Production, School of Veterinary Medicine, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy cDepartment of MCA Biology, University of Camerino, Via Gentile III da Varano, 62032 Camerino MC, Italy ARTICLE INFO ABSTRACT Article history: In order to gain more knowledge on the stress responses of gilhead seabream (Sparus aurata) Received 29 February 2008 under extreme conditions, this study investigated the functional properties of the Received in revised form 19 May 2008 hemoglobin system and globin gene expression under hypoxia and low salinity. The Accepted 20 May 2008 oxygen affinity for the two hemoglobin components present inside the S. aurata erythrocyte Available online 27 June 2008 was practically identical as was the influence of protons and organic phosphates (Root effect). The quantification of S. aurata hemoglobin fractions performed by HPLC and the data Keywords: on gene expression of globin chains assayed by PCR indicate that under hypoxia and low Hemoglobins salinity there is a change in the ratio between the two different hemoglobin components. Root effect The result indicating that the distinct hemoglobins present in S. aurata erythrocyte have Globins almost identical functional properties, does not explain the adaptive response (expression Gene expression change) following exposure of the animal to hypoxia or low salinity on the basis of their Salinity function as oxygen transporter. We hypothesize that other parallel biological functions that Hypoxia the hemoglobin molecule is known to display within the erythrocyte are involved in adaptive molecular mechanisms. The autoxidation–reduction cycle of hemoglobin could be involved in the response to particular living conditions. © 2008 Elsevier B.V. All rights reserved. 1. Introduction influenced by different effectors such as chlorides, protons (Bohr effect), CO2 and organic phosphates. All these effectors The functional properties of hemoglobin are characterized by bind preferentially to the T state of hemoglobin lowering the the presence of both homotropic and heterotropic interaction overall O2 affinity of the molecule. phenomena which have been studied over the years. Many fish species have multiple Hb components and this Cooperativity between subunits is achieved through the Hb multiplicity is related to the greater variability in oxygen conformational transition between the deoxy-low-affinity regimes to which animals are subjected to. The presence of state (or T state) and the oxy-high-affinity state (or R state), different hemoglobin components correlates also with the role which accounts for the sigmoidal shape of the oxygen binding of O2 release against high hydrostatic pressure inside the curve. In addition, the oxygen affinity of hemoglobin is swim bladder. Hemoglobins involved in this function display a ⁎ Corresponding author. Tel.: +39 0737 403211; fax: +39 0737 403290. E-mail address: [email protected] (G. Falcioni). 0048-9697/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2008.05.027 SCIENCE OF THE TOTAL ENVIRONMENT 403 (2008) 148– 153 149 very marked Bohr effect (called Root effect). The oxygen Three adult globin genes have been found in S. aurata; two binding properties of Hbs that exhibit Root effect are different α-globin genes and one β-globin gene have been characterized by a very strong dependence of both affinity identified and their nucleotide and aminoacid sequences have and cooperativity on pH and organic phosphates. The already been submitted to the GeneBank database (accession essential feature of this phenomenon appears to be a proton numbers DQ520839; DQ520840 and DQ452379 respectively). induced stabilization of the low affinity state of the molecule The oxygen binding properties of the two purified hemoglobin (Brunori, 1975). At the structural level, the Root effect has been components as a function of pH and organic phosphates were correlated (Perutz and Brunori, 1982) with two additional H- also investigated. bonds involving the protonated form of His HC3 (146β) and a serine in position F9 (93β) which, in Root effect hemoglobins, substitutes the cysteinyl residue normally found in mammals. 2. Materials and methods Comparative studies on the structural and functional properties of hemoglobins permit to speculate on the adaptive 2.1. Sample collection molecular mechanisms developed to satisfy particular needs of oxygen demand due to different environmental conditions Six specimens of S. aurata obtained from an Ippocampus fish- to which animals may be subjected to. Environmental factors farmer (Villafranca Tirrena, ME, Italy) were stabulated into a can include variations in temperature, pH, salinity, oxygen 300 L aquarium under standard conditions, at the temperature tension, etc. of 20 °C, and pH 8.0. The concentration of oxygen was kept In intensive fish culture systems, a reduced availability of at 6.5–7.0 mg/L (Titolation kit — Hanna, USA), by a pump dissolved oxygen in water is often observed. This is ascribed to oxygenator, whereas the nitrates/nitrites were monitored and a high fish density and to the feeding practices; algal blooms maintained below 0.05 mg/L (Ascol test, Read Sea, and and elevated temperatures can contribute as well. Nitrification Active Bacteria kit — Aquaristica, Italy). After This lack of oxygen can induce responses and the typical 10 days stabulation, blood was collected from the caudal vein metabolic adjustments caused by the hypoxic stress are to of each specimen, using MS-222 40 mg/L as anesthetic, for no maintain oxygen supplies in the critical organs and to reduce longer than 4 min, and 50 mM Na2EDTA as anticoagulant. consumption of oxygen. Blood samples were immediately processed. In order to cope with periods of hypoxia, many fish species Subsequently, the fishes were stabulated for an additional have evolved new molecular responses (Nikinmaa, 2002; 20 days during which oxygen concentration was progressively Nilsson and Renshaw, 2004; Cossins and Crawford, 2005; reduced to 2.5 mg/L towards the end. A new blood sample was Nikinmaa and Rees, 2005). Some adaptive mechanisms can then collected under the same conditions. change fish gene expression with the aim of saving oxygen Finally, the fishes were stabulated for further 20 days at (Gracey et al., 2001; Ton et al., 2003; Van der Meer et al., 2005). normal oxygen concentration, while progressively reducing the The patterns of hypoxic differential gene expression are not salt concentration from normal 38 ppm to 28 ppm. The third well known. Understanding the tissue-specific and temporal blood sample was then collected under the same conditions. changes in gene expression in fishes exposed to hypoxia could reveal new mechanisms of tolerance to the lack of oxygen and 2.2. Separation of homogeneous hemoglobin components they could shed light on the evolution of this adaptive by preparative column chromatography response in vertebrates. Hemoglobin and myoglobin are respiratory proteins that link and store oxygen. Under hypoxic To obtain purified Hb components, a total of about 4 mL of conditions gene expression of globins could be modified. blood was collected from different animals. Blood from sea Salinity can also contribute to increase environmental bream S. aurata was withdrawn from the caudal vein into an stress. Most fish live in an osmotic disequilibrium between the isotonic medium constituted by 0.1 M phosphate buffer, 0.1 M environment and their blood plasma and body tissues, there- NaCl, 0.2% citrate, 1 mM EDTA, pH 7.8. The red blood cells were fore they must be able to maintain an internal osmotic separated from the plasma by centrifugation for 10 min at environment across a wide range of salinity. Alterations in 1000 g and were washed four times with the same isotonic the environmental amount of salt may affect electrolyte levels buffer. Hemolysis was accomplished by adding 3 volumes of − (i.e. Na+ and Cl ) and, as a consequence, the acid–base balance distilled water to the red cells; after 30 min the solution was (Junsen et al., 1998). centrifuged for 20 min at 10,000 g and the supernatant was There is enormous variety in the types of environmental dialysed against 0.1 M Tris–HCl buffer at pH 9.1 containing − stressors; it is generally agreed that stress in fish evokes an EDTA 5 ×10 4 M. The solution of hemoglobin previously ordered sequence of well-defined physiological changes. dialysed was applied to a DEAE (diethylaminoethylcellulose) The Sparidae Family occupies an important position Sephadex A-50 column (dimensions 40×2 cm) equilibrated among the Teleostei of the Mediterranean basin. In fact, with the same buffer. A pH gradient elution was carried out some fishes of this Family have a special role in the using two containers, one with 250 mL of 0.1 M Tris–HCl − gastronomic, industrial and economic fields. Amongst the buffer +EDTA 5×10 4 M at pH 9.1 under stirring and the other different species, Sparus aurata is the most capable of adapting with 1 L of 0.1 M KH2PO4, the former being connected directly to different environmental conditions, like those of fish farms. to the column. The flow rate was maintained at about 30– The aim of this study was to investigate the stress responses 40 mL/h; 3–4 mL fractions were collected. Representative of S. aurata under hypoxia and low salinity, in particular with fractions were examined by cellulose acetate electrophoresis regards to the hemoglobin system and globin gene expression.
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