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Aerobic Mitochondrial Capacities in Antarctic and Temperate Eelpout (Zoarcidae) Subjected to Warm Versus Cold Acclimation

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Aerobic Mitochondrial Capacities in Antarctic and Temperate Eelpout (Zoarcidae) Subjected to Warm Versus Cold Acclimation Polar Biol (2005) 28: 575–584 DOI 10.1007/s00300-005-0730-9 ORIGINAL PAPER Gisela Lannig Æ Daniela Storch Æ Hans-O. Po¨rtner Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation Received: 3 September 2004 / Revised: 15 February 2005 / Accepted: 3 March 2005 / Published online: 15 April 2005 Ó Springer-Verlag 2005 Abstract Capacities and effects of cold or warm Introduction acclimation were investigated in two zoarcid species from the North Sea (Zoarces viviparus) and the Ant- The geographical distribution of ectothermic species is arctic (Pachycara brachycephalum) by investigating related to the ambient temperature regime, and toler- temperature dependent mitochondrial respiration and + ance to fluctuations of habitat temperature exists only activities of citrate synthase (CS) and NADP within certain limits (for review see Portner 2001; -dependent isocitrate dehydrogenase (IDH) in the liver. ¨ Po¨ rtner 2002a). Living in extreme Antarctic environ- Antarctic eelpout were acclimated to 5°C and 0°C ment appears to be associated with reduced tolerance (controls) for at least 10 months, whereas boreal eel- to higher temperatures. Low upper-lethal temperatures pout, Z. viviparus (North Sea) were acclimated to 5°C have been observed in the Antarctic brachiopod, and to 10°C (controls). Liver sizes were found to be Liothyrella uva between 3 C and 4.5 C (Peck 1989). increased in both species in the cold, with a concom- ° ° Portner et al. (1999a) found a short-term upper lethal itant rise in liver mitochondrial protein content. As a ¨ temperature of 4 C and a long-term upper limit of result, total liver state III rates were elevated in both ° around 2 C in the bivalve Limopsis marionensis.An cold-versus and warm-exposed P. brachycephalum and ° upper-lethal temperature of 6 C was found in three Z. viviparus, with the highest rates in boreal eelpout ° species of the Antarctic fish Trematomus by Somero acclimated to 5°C. CS and IDH activities in the total and de Vries (1967). Antarctic eelpout, Pachycara liver were similar in Z. viviparus acclimated to 5°C and brachycephalum and the Notothenioid, Lepidonotothen 10°C, but decreased in those warm acclimated versus nudifrons survived temperatures of up to 9–10 C (van control P. brachycephalum. Enzyme capacities in the ° Djik et al. 1999; Hardewig et al. 1999), and Mark total liver were higher in eelpout from Antarctica than et al. (2002) reported a lethal temperature of those from the North Sea. In conclusion, cold com- P. brachycephalum at around 13 C. Reduced heat pensation of aerobic capacities in the liver seems to be ° tolerance in cold-stenothermal ectotherms is likely linked to an increase in organ size with unchanged linked to cold induced functional adaptations, which specific mitochondrial protein content. Despite its life compensate for the decelerating effect of low temper- in permanently cold climate, P. brachycephalum was atures on metabolic processes. able to reduce liver aerobic capacities in warm climate Mitochondrial proliferation has been found in cold and thus, displayed a capacity for temperature accli- adapted Southern and Northern hemisphere species mation. (Londraville and Sidell 1990; Johnston et al. 1998; Sommer and Po¨ rtner 2002) as well as in cold acclimated eurythermal species (Campbell and Davies 1978; Egginton and Sidell 1989). Furthermore, enhanced enzyme activities are found in cold adapted as well as in cold acclimated animals (Crockett and Sidell 1990; G. Lannig (&) Æ D. Storch Æ H.-O. Po¨ rtner Sokolova and Po¨ rtner 2001; Kawall et al. 2002; Lannig Alfred Wegener Institute for Marine and Polar Research, et al. 2003). Besides enhanced mitochondrial densities, Am Handelshafen 12, 27570 an increase in total organ size has also been reported to Bremerhaven, Germany compensate for the effects of low temperatures (Kent E-mail: [email protected] Tel.: +49-471-48311288 et al. 1988 (liver and heart); Seddon and Prosser 1997 Fax: +49-471-48311149 (liver); Lannig et al. 2003 (liver)). 576 Despite compensatory increase in tissue aerobic placed in the same aquarium at 5±0.5°C and a salinity capacities, Antarctic animals show uncompensated of 34&. Other animals remained at control tempera- resting metabolic rates (Clarke 1991; van Dijk et al. tures. All animals were kept under a 12:12-h light–dark 1999; for review see Po¨ rtner et al. 2000; Peck 2002) and cycle and fed live shrimp once per week. Experiments uncompensated specific maximal respiration rates of were carried out at the start of 2003, after an acclimation mitochondria (Johnston et al. 1994; Johnston et al. 1998; period at 5°C of at least 10 months. Po¨ rtner et al. 1999b; Hardewig et al. 1999). Po¨ rtner et al. (2000) suggested that mitochondrial and whole animal aerobic capacities remain uncompensated only in cold- Preparation of mitochondria stenothermal organisms, as opposed to cold adapted eurytherms. This may also be associated with the The isolation of mitochondria was modified after inability of cold-stenotherms to acclimate to warmer Hardewig et al. (1999). After the fish were killed, the temperatures (e.g. Weinstein and Somero 1998). liver was removed immediately, chopped finely with The adjustment of aerobic scope by setting mito- scissors in an ice-cold glass dish, and extracted in 10– chondrial densities and capacities is seen as a crucial step 25 ml of homogenisation buffer, depending on liver wet in shifting thermal tolerance windows (cf. Po¨ rtner mass, approximately 0.5 g per 10 ml (50 mM Hepes, 2002a). The present study was designed to investigate 80 mM sucrose, 85 mM KCl, 5 mM EDTA, 5 mM the ability to adjust aerobic metabolism to changing EGTA, pH 7.1 (20°C) with freshly added 1% BSA and À1 temperature in Antarctic compared to temperate eury- 1 llml aprotinin) with a Potter-Elvejhem homogen- thermal fish. We wanted to investigate whether a iser. After centrifugation (12 min at 400 g and 0°C) the demersal Antarctic species like P. brachycephalum is able pellet was re-homogenised in the same volume of to undergo adjustments in aerobic metabolism to vari- homogenisation buffer and centrifuged again. The ous temperatures despite living in a cold-stable envi- combined supernatants were centrifuged for 8 min at ronment. If so, the question arises whether the patterns 10,000 g and 0°C. The mitochondrial pellet was re- of temperature compensation are similar for stenother- suspended in 1–2 ml assay medium (50 mM Hepes, mal and eurythermal ectotherms. Accordingly, the re- 85 mM KCl, 80 mM sucrose, 5 mM KH2PO4, pH 7.1 À1 sponse to a 5°C temperature change was compared in (20°C) with freshly added 1% BSA and 1llml ap- closely related members of the zoarcid fish family. We rotinin). In some cases the livers of two animals were acclimated cold adapted Antarctic eelpout, P. brachy- pooled to enhance the volume of mitochondrial sus- cephalum, from 0°Cto5°C, whereas temperate common pension but counted as one in the statistical analyses North Sea eelpout, Zoarces viviparus were acclimated and results. from 5°Cto10°C. We investigated mitochondrial res- piration rates and the enzyme activities of citrate syn- thase (CS) and NADP+ -dependent isocitrate Mitochondrial respiration and enzyme assays dehydrogenase (IDH) in liver mitochondria at different temperatures. CS was chosen as an indicator of citric Mitochondrial oxygen consumption was measured at acid cycle activity and IDH as representing a key role in different temperatures (5, 8, 10, 15 and 20°C) using a a mitochondrial substrate cycle, which may be relevant Clark-type oxygen electrode in a thermostatted respira- in the control of mitochondrial respiration, redox status tion chamber (Eschweiler, Kiel). A total of 100 ll of the and proton leakage (Sazanov and Jackson 1994;Po¨ rtner mitochondrial suspension were combined with assay et al. 1999b). medium, without BSA and aprotinin, to a total volume of 1 ml, containing 0.5–1.2 mg mitochondrial protein per millilitre, 5 lM di-adenosine pentaphosphate Materials and methods (Ap5A, an inhibitor of myokinase) and 3.3 mM succi- nate as a substrate since respiration showed lower rates Animals using pyruvate and malate. State III respiration was recorded after addition of 0.3 mM ADP and state VI Antarctic eelpout, P. brachycephalum were caught by respiration was determined after all ADP had been baited traps close to King George Island (depth 397– phosphorylated. Finally, the respiration induced by 455 m) during the RV Polarstern Antarctic expedition proton leakage (state IVol) was recorded after adding XV/3 1998. The fish were kept in aquaria onboard the 2.5 lgmlÀ1 oligomycin, an inhibitor of mitochondrial RV Polarstern and later at the Alfred Wegener Institute F0F1-ATPase. P/O ratios were calculated by classical (Bremerhaven) at ambient temperatures of 0±0.5°C and determination according to Chance and Williams (1956). a salinity of 34&. North Sea eelpout, Z. viviparus were Mitochondrial oxygen consumption was calculated as caught in the German Bight near Helgoland (in August nanomole O minÀ1 mg proteinÀ1 by adopting values of 2001 and in March 2002) and kept in aquaria at the oxygen solubility in the assay medium from Johnston Alfred Wegener Institute at temperatures of 10±1°C et al. (1994). Protein concentration was determined by and a salinity of 34&. Acclimation to 5°C started in the Biuret method after Gornall et al. (1949) using 5% spring 2002, with Antarctic and North Sea eelpouts deoxycholate to solubilize membrane proteins. 577 Since the high lipid content in liver disturbed the mitochondrial protein content, mitochondrial respira- photometric measurements, 3 M TCA was used to pre- tion rates and enzyme activities for total liver, normal- cipitate and separate the protein by centrifugation for ized to a 40 g eelpout (see Pelletier et al.
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