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Mitochondrial oxyconformity and cold adaptation in the polychaete Nereis pelagica and the bivalve Arctica islandica from the Baltic and White Seas
K. Tschischka, D. Abele, H.O. Portner
Journal of Experimental Biology 2000 203: 3355-3368;

Summary

The rates of oxygen uptake of the marine polychaete Nereis pelagica and the bivalve Arctica islandica depend on the availability of ambient oxygen. This is manifest both at the tissue level and in isolated mitochondria studied between oxygen tensions (P(O2)) of 6.3 and 47.6 kPa (47–357 mmHg). Oxyconformity was found in both Baltic Sea (Kiel Bight) and cold-adapted White Sea populations of the two species. However, mitochondria isolated from White Sea specimens of N. pelagica and A. islandica showed a two- to threefold higher aerobic capacity than mitochondria prepared from Baltic Sea specimens. We tested whether mitochondrial oxyconformity can be explained by an additional electron pathway that is directly controlled by P(O2). Mitochondrial respiration of both invertebrate species was inhibited by cyanide (KCN) and by salicylhydroxamic acid (SHAM). The overall rate of mitochondrial oxygen consumption increased at high P(O2). Phosphorylation efficiency (ADP/O ratio) decreased at elevated P(O2) (27.5-47.6 kPa, 206–357 mmHg), regardless of whether malate or succinate was used as a substrate. In contrast to the invertebrate mitochondria studied, mitochondria isolated from bovine heart, as an oxyregulating control species, did not show an elevated rate of oxygen uptake at high P(O2) in any respiratory state, with the exception of state 2 malate respiration. In addition, rates of ATP formation, respiratory control ratios (RCR) and ADP/O ratios remained virtually unchanged or even tended to decreased. In conclusion, the comparison between mitochondria from oxyregulating and oxyconforming organisms supports the existence of an alternative oxidase in addition to the classical cytochrome c oxidase. In accordance with models discussed previously, oxidative phosphorylation does not explain the rate of mitochondrial oxygen consumption during progressive activation of the alternative electron transport system. We discuss the alternative system, thought to be adaptive in confined, usually hypoxic environments, where excess oxygen can be eliminated and oxygen levels can be kept low by an increase in the rate of oxygen consumption, thereby minimizing the risk of oxidative stress.

REFERENCES

    1. Bahr, J. T. and
    2. Bonner, W. D.
    (1973). Cyanide-insensitive respiration. I. The steady states of skunk cabbage spadix and bean hypocotyl mitochondria. J. Biol. Chem 248, 3441–.
    OpenUrlAbstract/FREE Full Text
    1. Bayne, B. L.
    (1971). Oxygen consumption by three species of lamellibranch mollusc in declining oxygen tension at reduced salinity. Comp. Biochem. Physiol 40, 955–.
    OpenUrlCrossRef
    1. Bertsova, Y. V.,
    2. Bogachev, A. V. and
    3. Skulachev, V. P.
    (1997). Generation of protonic potential by the bd-type quinol oxidase of Azotobacter vinlandii. FEBS Lett 414, 369–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Bingham, I. J. and
    2. Stevenson, E. A.
    (1995). Causes and location of non-specific effects of SHAM on O2uptake by wheat roots. Physiol. Plant 93, 427–.
    OpenUrlCrossRef
    1. Boveris, A.,
    2. Martino, E. and
    3. Stoppani, A. O. M.
    (1977). Evaluation of the horseradish peroxidase—scopoletin method for the measurement of hydrogen peroxide formation in biological systems. Analyt. Biochem 80, 145–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Brand, M. D.
    (1990). The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J. Theor. Biol 145, 267–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Brand, M. D.,
    2. Chien, L.-F.,
    3. Ainscow, E. K.,
    4. Rolfe, D. F. S. and
    5. Porter, R. K.
    (1994). The causes and function of mitochondrial proton leak. Biochim. Biophys. Acta 1187, 132–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Brierley, G. P.,
    2. Jurkowitz, M. S.,
    3. Farooqui, T. and
    4. Jung, G. W.
    (1984). K+/H+antiport in heart mitochondria. J. Biol. Chem 259, 14672–.
    OpenUrlAbstract/FREE Full Text
    1. Brookes, P. S.,
    2. Buckingham, J. A.,
    3. Tenreiro, A. M.,
    4. Hulbert, A. J. and
    5. Brand, M. D.
    (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 119, 325–.
    1. Chance, B. and
    2. Williams, G. R.
    (1955). Respiratory enzymes in oxidative phosphorylation. I. Kinetics of oxygen utilization. J. Biol. Chem 217, 383–.
    OpenUrlFREE Full Text
    1. Cheah, K. S.
    (1973). The oxidase system of Monieza expansa (Cestoda). Comp. Biochem. Physiol 23, 277–.
    OpenUrl
    1. D'Mello, R.,
    2. Hill, S. and
    3. Poole, R. K.
    (1994). Determination of the oxygen affinities of terminal oxidases in Azotobacter vinlandii using the deoxygenation of oxyleghaemoglobin and oxymyoglobin: cytochrome bd is a low-affinity oxidase. Microbiol 140, 1395–.
    OpenUrlCrossRef
    1. Estabrook, R. W.
    (1967). Mitochondrial respiratory control and the polarographic measurements in mitochondria. Meth. Enzymol 10, 41–.
    OpenUrlCrossRef
    1. Freeman, B. A. and
    2. Crapo, J. D.
    (1981). Hyperoxia increase oxygen radical production in rat lungs and lung mitochondria. J. Biol. Chem 256, 10986–.
    OpenUrlFREE Full Text
    1. Gnaiger, E.,
    2. Steinlechner-Maran, R.,
    3. Mendez, G.,
    4. Eberl, T. and
    5. Margreiter, R.
    (1995). Control of mitochondrial and cellular respiration by oxygen. J. Bioenerg. Biomembr 27, 583–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Goyal, N. and
    2. Srivastava, V. M. L.
    (1995). Oxidation and reduction of cytochrome c by mitochondrial enzymes of Setaria cervi. J. Helminthol 69, 13–.
    OpenUrlPubMed
    1. Hafner, R. P.,
    2. Brown, G. C. and
    3. Brand, M. D.
    (1990). Analysis of the control of respiration rate, phosphorylation rate, proton leak rate and protonmotive force in isolated mitochondria using the ‘top-down’ approach of metabolic control theory. Eur. J. Biochem 188, 313–.
    OpenUrlPubMedWeb of Science
    1. Hand, S. C. and
    2. Somero, G. M.
    (1983). Energy metabolic pathways3368of hydrothermal vent animals: Adaptation to food-rich and sulfide-rich deep-sea environments. Biol. Bull 165, 167–.
    OpenUrlAbstract/FREE Full Text
    1. Khazanov, V. A.,
    2. Poborsky, A. N. and
    3. Kondrashova, M. N.
    (1992). Air saturation of the medium reduces the rate of phosphorylating oxidation of succinate in isolated mitochondria. FEBS Lett 314, 264–.
    OpenUrlCrossRefPubMed
    1. Masini, A.,
    2. Ceccarelli-Stanzani, D. and
    3. Muscatello, U.
    (1983). Phosphorylating efficiency of isolated rat liver mitochondria respiring under the conditions of steady-state 4. Biochim. Biophys. Acta 724, 251–.
    OpenUrlPubMed
    1. Mendis, A. H. W. and
    2. Evans, A. A. F.
    (1984). First evidence for the occurrence of cytochrome o in a free-living nematode. Comp. Biochem. Physiol 78, 729–.
    OpenUrlCrossRef
    1. Minghetti, K. C. and
    2. Gennis, R. B.
    (1988). The two terminal oxidases of the aerobic respiratory chain of Escherichia coli each yield water and not peroxide as a final product. Biochem. Biophys. Res. Commun 155, 243–.
    OpenUrlCrossRefPubMed
    1. Moyes, C. D.,
    2. Moon, T. W. and
    3. Ballantyne, J. S.
    (1985). Glutamate catabolism in mitochondria from Mya arenaria mantle: Effects of pH on the role of glutamate dehydrogenase. J. Exp. Zool 236, 293–.
    OpenUrlCrossRef
    1. Njogu, R. M.,
    2. Whittaker, C. J. and
    3. Hill, D. C.
    (1980). Evidence for a branched electron transport chain in Trypanosoma brucei. Mol. Biochem. Parasitol 1, 13–.
    OpenUrlCrossRefPubMed
    1. O'Brien, J. and
    2. Vetter, R. D.
    (1990). Production of thiosulphate during sulphide oxidation by mitochondria of the symbiont-containing bivalve Solemya reidi. J. Exp. Biol 149, 133–.
    OpenUrlAbstract/FREE Full Text
    1. Oshino, N.,
    2. Sugano, T. R.,
    3. Oshino, R. and
    4. Chance, B.
    (1974). Mitochondrial function under hypoxic conditions: The steady states of cytochrome a + a 3and their relation to mitochondrial energy states. Biochim. Biophys. Acta 368, 298–.
    OpenUrlPubMedWeb of Science
    1. Paget, T. A.,
    2. Fry, M. and
    3. Lloyd, D.
    (1987). Effects of inhibitors on the oxygen kinetics of Nippostrongylus brasiliensis. Mol. Biochem. Parasitol 22, 125–.
    OpenUrlCrossRefPubMed
    1. Paget, T. A.,
    2. Fry, M. and
    3. Lloyd, D.
    (1987). Hydrogen peroxide production in uncoupled mitochondria of the parasitic nematode worm Nippostrongylus brasiliensis. Biochem. J 243, 589–.
    OpenUrlAbstract/FREE Full Text
    1. Paget, T. A.,
    2. Fry, M. and
    3. Lloyd, D.
    (1988). Haemoprotein terminal oxidases in the nematodes Nippostrongylus brasiliensis and Ascaridia galli. Biochem. J 256, 295–.
    OpenUrlAbstract/FREE Full Text
    1. Paget, T. A.,
    2. Fry, M. and
    3. Lloyd, D.
    (1988). The O2-dependence of respiration and H2O2production in the parasitic nematode Ascaridia galli. Biochem. J 256, 633–.
    OpenUrlAbstract/FREE Full Text
    1. Popov, V. N.,
    2. Simonian, R. A.,
    3. Skulachev, V. P. and
    4. Starkov, A. A.
    (1997). Inhibition of the alternative oxidase simulates H2O2production in plant mitochondria. FEBS Lett 415, 87–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Pörtner, H. O.,
    2. Heisler, N. and
    3. Grieshaber, M. K.
    (1985). Oxygen consumption and mode of energy production in the intertidal worm Sipunculus nudus L.: definition and characterization of the critical P Ofor an oxyconformer. Respir. Physiol 59, 361–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Schonbaum, G. R.,
    2. Bonner, W. D.,
    3. Storey, B. T. and
    4. Bahr, J. T.
    (1971). Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol 47, 124–.
    OpenUrlAbstract/FREE Full Text
    1. Schroff, G. and
    2. Schöttler, U.
    (1977). Anaerobic reduction of fumarate in the body wall musculature of Arenicola marina (Polychaeta). J. Comp. Physiol 116, 325–.
    OpenUrl
    1. Shumway, S. E.
    (1979). The effects of body size, oxygen tension and mode of life on the oxygen uptake rates of polychaetes. Comp. Biochem. Physiol 64, 273–.
    OpenUrlCrossRef
    1. Skulachev, V. P.
    (1996). Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q. Rev. Biophys 29, 169–.
    OpenUrlCrossRefPubMedWeb of Science
    1. Taylor, A. C. and
    2. Brand, A. R.
    (1975). A comparative study of the respiratory responses of the bivalves Arcticaislandica (L.) and Mytilus edulis (L.) to declining oxygen tension. Proc. R. Soc. Lond. B 190, 443–.
    OpenUrlPubMed
    1. Webster, D. A.
    (1975). The formation of hydrogen peroxide during the oxidation of reduced nicotinamide adenine dinucleotide by cytochrome o from Vitreoscilla. J. Biol. Chem 250, 4955–.
    OpenUrlAbstract/FREE Full Text
    1. Wibom, R.,
    2. Lundin, A. and
    3. Hultman, E.
    (1990). A sensitive method for measuring ATP-formation in rat muscle mitochondria. Scand. J. Clin. Lab. Invest 50, 143–.
    OpenUrlPubMedWeb of Science
    1. Wieser, W.
    (1985). Developmental and metabolic constraints of the scope of activity in young rainbow trout (Salmo gairdneri). J. Exp. Biol 118, 133–.
    OpenUrlAbstract/FREE Full Text
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Journal Articles
Mitochondrial oxyconformity and cold adaptation in the polychaete Nereis pelagica and the bivalve Arctica islandica from the Baltic and White Seas
K. Tschischka, D. Abele, H.O. Portner
Journal of Experimental Biology 2000 203: 3355-3368;
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