Skip to main content

Advertisement

Log in

Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Capacities and effects of cold or warm acclimation were investigated in two zoarcid species from the North Sea (Zoarces viviparus) and the Antarctic (Pachycara brachycephalum) by investigating temperature dependent mitochondrial respiration and activities of citrate synthase (CS) and NADP+ -dependent isocitrate dehydrogenase (IDH) in the liver. Antarctic eelpout were acclimated to 5°C and 0°C (controls) for at least 10 months, whereas boreal eelpout, Z. viviparus (North Sea) were acclimated to 5°C and to 10°C (controls). Liver sizes were found to be increased in both species in the cold, with a concomitant rise in liver mitochondrial protein content. As a result, total liver state III rates were elevated in both cold-versus and warm-exposed P. brachycephalum and Z. viviparus, with the highest rates in boreal eelpout acclimated to 5°C. CS and IDH activities in the total liver were similar in Z. viviparus acclimated to 5°C and 10°C, but decreased in those warm acclimated versus control P. brachycephalum. Enzyme capacities in the total liver were higher in eelpout from Antarctica than those from the North Sea. In conclusion, cold compensation of aerobic capacities in the liver seems to be linked to an increase in organ size with unchanged specific mitochondrial protein content. Despite its life in permanently cold climate, P. brachycephalum was able to reduce liver aerobic capacities in warm climate and thus, displayed a capacity for temperature acclimation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alp RP, Newshole EA, Zammit VA (1976) Activities of citrate synthetase and NAD+-linked and NADP+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. Biochem J 154:689–700

    Google Scholar 

  • Anderson ME (1994) Systematics and Osteology of the Zoarcidae (Teleostei: Perciformes). Ichthyol Bull 60:120

    Google Scholar 

  • Blier PU, Guderley H (1993) Mitochondrial activity in rainbow trout red muscle: the effect of temperature on the ADP-dependence of ATP synthesis. J Exp Biol 176:145–157

    Google Scholar 

  • Blier PU, Lemieux H (2001) The impact of the thermal sensitivity of cytochrome c oxidase on the respiration rate of Arctic charr red muscle mitochondria. J Comp Physiol B 171:247–253

    Google Scholar 

  • Brand MD (1990) The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J Theor Biol 145:267–286

    Google Scholar 

  • Brand MD, Chien LF, Ainscow EK, Rolfe DFS, Porter RK (1994) The causes and functions of mitochondrial proton leak. Biochem Biophys Acta 1187:132–139

    Google Scholar 

  • Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD (1998) The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B 119:325–334

    Article  CAS  PubMed  Google Scholar 

  • Campbell C, Davies P (1978) Temperature acclimation in the teleost, Blennius pholis: changes in enzyme activity and cell structure. Comp Biochem Physiol B 61:165–167

    Google Scholar 

  • Chance B, Williams GR (1956) The respiratory chain and oxidative phosphorylation. Adv Enzymol 17:65–134

    Google Scholar 

  • Clarke A (1991) What is cold compensation and how should we measure it? Am Zool 31:81–92

    Google Scholar 

  • Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol Zool 63:472–488

    Google Scholar 

  • van Dijk PLM, Tesch C, Hardewig I, Pörtner HO (1999) Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202:3611–3621

    Google Scholar 

  • Eastman J (1993) Antarctic fish biology: evolution in a unique environment. Academic, San Diego

    Google Scholar 

  • Egginton S, Sidell B (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:R1–R10

    Google Scholar 

  • Ellory JC, Hall AC (1987) Temperature effects on red cell membrane transport processes. In: Bowler K, Fuller BJ (eds.) Temperature and animal cells. Symp Soc Exp Biol 31:53–66

    Google Scholar 

  • Fischer T (2002) The effects of climate induced temperature changes on cod (Gadus morhua L.): linking ecological and physiological investigations. PhD Thesis, University Bremen

  • Gonzalez-Cabrera PJ, Dowd F, Pedibhotla VK, Rosario R, Stanley-Samuelson D, Petzel D (1995) Enhanced hypo-osmoregulation induced by warm-acclimation in Antarctic fish mediated by increased gill and kidney Na+/K+ -ATPase activities. J Exp Biol 198:2279–2291

    Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of biuret reaction. J Biol Chem 117:751–66

    Google Scholar 

  • Guderley H (1998) Temperature and growth rates as modulators of the metabolic capacities of fish muscle. In: Pörtner HO, Playle R (eds.) Cold ocean physiology. Cambridge University Press, London, pp 58–87

    Google Scholar 

  • Hardewig I, Peck LS, Pörtner HO (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons. J Comp Physiol B 169:597–604

    Google Scholar 

  • Johnston IA, Guderley H, Franklin CE, Crockford T, Kamunde C (1994) Are mitochondria subject to evolutionary temperature adaptations?. J Exp Biol 195:293–306

    Google Scholar 

  • Johnston IA, Calvo J, Guderley H, Fernandez D, Palmer L (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12

    Google Scholar 

  • Kawall HG, Torres JJ, Sidell BD, Somero GN (2002) Metabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain. Mar Biol 140:279–286

    Google Scholar 

  • Kent J, Koban M, Prosser C (1988) Cold-acclimation induced protein hypertrophy in channel catfish and green sunfish. J Comp Physiol B 158:185–198

    Google Scholar 

  • Lannig G, Eckerle LG, Serendero I, Sartoris FJ, Fischer T, Knust R, Johansen T, Pörtner HO (2003) Temperature adaptation in eurythermal cod (Gadus morhua): a comparison of mitochondrial enzyme capacities in boreal and Arctic populations. Mar Biol 142:589–599

    Google Scholar 

  • Londraville R, Sidell B (1990) Ultrastructure of aerobic muscle in Antarctic fishes may contribute to maintenance of diffusion fluxes. J Exp Biol 150:205–220

    Google Scholar 

  • Lucassen M, Schmidt A, Eckerle LG, Pörtner HO (2003) Mitochondrial proliferation in the permanent versus temporary cold: enzyme activities and mRNA levels in Antarctic and temperate zoarcid fish. Am J Physiol Regul Integr Comp Physiol 258:1410–1420

    Google Scholar 

  • Mark FC, Bock C, Pörtner HO (2002) Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and 31P-MRS. Am J Physiol 283(5):R1254–R1262

    Google Scholar 

  • Moyes CD, Buck LT, Hochachka PW (1988) Temperature effects on pH of mitochondria isolated from carp red muscle. Am J Physiol 254(4):R611–R615

    Google Scholar 

  • Peck LS (1989) Temperature and basal metabolism of two Antarctic marine herbivores. J Exp Mar Biol Ecol 125:1–12

    Google Scholar 

  • Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40

    Article  Google Scholar 

  • Pelletier D, Guderley H, Dutil JD (1993) Does the aerobic capacity of fish muscle change with growth rates? Fish Physiol Biochem 12:83–93

    Google Scholar 

  • Pörtner HO (2001) Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146

    Article  PubMed  Google Scholar 

  • Pörtner HO (2002a) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761

    Google Scholar 

  • Pörtner HO (2002b) Physiological basis of temperature dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230

    Google Scholar 

  • Pörtner HO, Peck LS, Zielinski S, Conway LZ (1999a) Intracellular pH and energy metabolism in the highly stenothermal Antarctic bivalve Limopsis marionensis as a function of ambient temperature. Polar Biol 22:17–30

    Article  Google Scholar 

  • Pörtner HO, Hardewig I, Peck LS (1999b) Mitochondrial function and critical temperature in the Antarctic bivalve, Laternula elliptica. Comp Biochem Physiol A 124:179–189

    Google Scholar 

  • Pörtner HO, van Dijk PLM, Hardewig I, Sommer A (2000) Levels of metabolic cold adaptation: tradeoffs in eurythermal and stenothermal ectotherms. In: Davison W, Williams CH (eds.) Antarctic ecosystems: models for wider ecological understanding. Caxton Press, Christchurch, pp 109–122

    Google Scholar 

  • Sazanov LA, Jackson JB (1994) Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett. 344:109–116

    Google Scholar 

  • Seddon W, Prosser C (1997) Seasonal variations in the temperature acclimation response of the channel catfish, Ictalurus punctatus. Physiol Zool 70:33–44

    Google Scholar 

  • Sidell W, Driedzic WR, Stowe DB, Johnston IA (1987) Biomedical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol Zool 60:221–232

    Google Scholar 

  • Sokolova IM, Pörtner HO (2001) Temperature effects on key metabolic enzymes in Littorina saxatilis and L. obtusata from different latitudes and shore levels. Mar Biol 139:113–126

    Google Scholar 

  • Somero GN, de Vries AL (1967) Temperature tolerance of some Antarctic fishes. Science 156:257–258

    CAS  PubMed  Google Scholar 

  • Sommer AM, Pörtner HO (2002) Metabolic cold adaptation in the lugworm Arenicola marina (L.): comparison of White Sea and a North Sea population. Mar Ecol Prog Ser 240:171–182

    Google Scholar 

  • van den Thillart G, Modderkolk J (1978) The effect of acclimation temperature on the activation energies of state III respiration and on the unsaturation of membrane lipids of goldfish mitochondria. Biochem Biophys Acta 510:38–51

    Google Scholar 

  • Torres J, Somero G (1988) Metabolism, enzymic activities and cold adaptation in Antarctic mesopelagic fishes. Mar Biol 98:169–180

    CAS  Google Scholar 

  • Weinstein RB, Somero GN (1998) Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernachii. J Comp Physiol 168:190–196

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank M. Lucassen for assistance in developing the stabilisation buffer for analysis of NADP+ -dependent isocitrate dehydrogenase activity, T. Hirse for support in protein determinations, and E. Brodte for her helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gisela Lannig.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lannig, G., Storch, D. & Pörtner, HO. Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation. Polar Biol 28, 575–584 (2005). https://doi.org/10.1007/s00300-005-0730-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-005-0730-9

Keywords

Navigation