Mitochondrial Acclimation Capacities to Ocean Warming and Acidification Are Limited in the Antarctic Nototheniid Fish, Notothenia rossii and Lepidonotothen squamifrons

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Strobel, Anneli ^a   Graeve, Martin ^a   Poertner, Hans O ^a   Mark, Felix C ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CITRIC ACID; FATTY ACID; PROTON; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ACIDIFICATION; ANIMAL CELL; ANIMAL TISSUE; ANTARCTICA; ARTICLE; BIOENERGY; BREATHING RATE; CITRIC ACID CYCLE; CONTROLLED STUDY; DECARBOXYLATION; ECOLOGY; ELECTRON TRANSPORT; ENVIRONMENTAL TEMPERATURE; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; FISH; HEAT ACCLIMATIZATION; HYPERCAPNIA; LEPIDONOTOTHEN SQUAMIFRONS; LIPID COMPOSITION; LIPID MEMBRANE; LIVER MITOCHONDRION; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; NONHUMAN; NOTOTHENIA ROSSII; OCEAN ENVIRONMENT; PLASTICITY; SPECIES HABITAT; THERMODYNAMICS; WARMING;

ACCLIMATIZATION; ACIDS; ANIMALS; ANTARCTIC REGIONS; CARBON DIOXIDE; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; GLOBAL WARMING; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; OCEANS AND SEAS; OXYGEN CONSUMPTION; PERCIFORMES; TEMPERATURE;

LEPIDONOTOTHEN SQUAMIFRONS; NOTOTHENIA ROSSII; NOTOTHENIIDAE;

EID: 84880021892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068865     Document Type: Article

References (72)

1. Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, et al. (2005) Antarctic climate change during the last 50 years. Int J Climatol 25: 279-294.
2. Turner J, Lachlan-Cope TA, Colwell S, Marshall GJ, Connolley WM, (2006) Significant warming of the Antarctic winter troposphere. Science 311: 1914-1917.
3. Meredith PM, King CJ, (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32: L196004.
4. Fuller A, Dawson T, Helmuth B, Hetem RS, Mitchell D, et al. (2010) Physiological Mechanisms in Coping with Climate Change. Physiol Biochem Zool 83: 713-720.
5. Egginton S, Sidell BD, (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol Regul Integr Comp Physiol 256: 1-9.
6. 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.
7. Hazel JR, (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57: 19-42.
8. Dey I, Buda C, Wiik T, Halver JE, Farkas T, (1993) Molecular and structural composition of phospholipid membranes in livers of marine and freshwater fish in relation to temperature. Proc Natl Acad Sci 90: 7498-7502.
9. Verde C, Parisi E, di Prisco G, (2006) The evolution of thermal adaptation in polar fish. Gene 385: 137-145.
10. Duchen MR, (1999) Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J Physiol 516: 1-17.
11. Poertner HO, (2002) 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.
12. Iftikar FI, MacDonald J, Hickey AJR, (2010) Thermal limits of portunid crab heart mitochondria: Could more thermo-stable mitochondria advantage invasive species? J Exp Mar Bio Ecol 395: 232-239.
13. Hilton Z, Clements KD, Hickey AJ, (2010) Temperature sensitivity of cardiac mitochondria in intertidal and subtidal triplefin fishes. J Comp Physiol B 180: 979-990.
14. Papetti C, Lio P, Ruber L, Patarnello T, Zardoya R, (2007) Antarctic fish mitochondrial genomes lack ND6 gene. J Mol Evol 65: 519-528.
15. Zhuang X, Cheng CH, (2010) ND6 gene "lost" and found: evolution of mitochondrial gene rearrangement in Antarctic notothenioids. Mol Biol Evol 27: 1391-1403.
16. Mark FC, Lucassen M, Strobel A, Barrera-Oro E, Koschnick N, et al. (2012) Mitochondrial Function in Antarctic Nototheniids with ND6 Translocation. PLoS Porter RK, Hulbert A, Brand MD (1996) Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol Regul Integr Comp Physiol 271: R1550-R1560.
17. Porter RK, Hulbert A, Brand MD, (1996) Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol Regul Integr Comp Physiol 271: R1550-R1560.
18. Brand M, (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 35: 811-820.
19. Chamberlin ME, (2004) Top-down control analysis of the effect of temperature on ectotherm oxidative phosphorylation. Am J Physiol Regul Integr Comp Physiol 287: R794-R800.
20. Jastroch M, Buckingham JA, Helwig M, Klingenspor M, Brand MD, (2007) Functional characterisation of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain J Comp Physiol B. 177: 743-752.
21. 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 19: 325-334.
22. Hardewig I, Peck LS, Poertner HO, (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid Lepidonotothen nudifrons. J Comp Physiol B 169: 597-604.
23. Trzcionka M, Withers KW, Klingenspor M, Jastroch M, (2008) The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J Exp Biol 211: 1911-1918.
24. Brand MD, Esteves TC, (2005) Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2: 85-93.
25. Keller M, Sommer A, Poertner HO, Abele D, (2004) Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes. J Exp Biol 207: 2529.
26. Heise K, Puntarulo S, Poertner HO, Abele D, (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp Biochem Physiol C 134: 79-90.
27. Mueller IA, Grim JM, Beers JM, Crockett EL, O'Brien KM, (2011) Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red-and white-blooded Antarctic notothenioid fishes. J Exp Biol 214: 3732-3741.
28. Brand M, Chien L, Ainscow E, Rolfe D, Porter R, (1994) The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187: 132.
29. Hazel JR, Williams E, (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29: 167.
30. Lee AG, (2004) How lipids affect the activities of integral membrane proteins. Biochim Biophys Acta 1666: 62-87.
31. Kraffe E, Marty Y, Guderley H, (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210: 149.
32. Deigweiher K, Koschnick N, Poertner HO, Lucassen M, (2008) Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. Am J Physiol Regul Integr Comp Physiol 295: R1660-R1670.
33. Eckerle LG, Lucassen M, Hirse T, Poertner HO, (2008) Cold induced changes of adenosine levels in common eelpout (Zoarces viviparus): a role in modulating cytochrome c oxidase expression. J Exp Biol 211: 1262-1269.
34. Windisch HS, Kathoever R, Poertner HO, Frickenhaus S, Lucassen M, (2011) Thermal acclimation in Antarctic fish: Transcriptomic profiling of metabolic pathways. Am J Physiol Regul Integr Comp Physiol 301: R1453-R1466.
35. Guderley H, St-Pierre J, (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205: 2237.
36. Lucassen M, Koschnick N, Eckerle, L G, Poertner HO, (2006) Mitochondiral mechanisms of cold adaptation in cod (Gadus morhua L.) populations from different climatic zones. J Exp Biol 209: 1410-1420.
37. Urschel M, O'Brien K, (2009) Mitochondrial function in Antarctic notothenioid fishes that differ in the expression of oxygen-binding proteins. Polar Biol 32: 1323-1330.
38. Weinstein RB, Somero GN, (1998) Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchii. J Comp Physiol B 168: 190-196.
39. Enzor LA, Zippay ML, Place SP, (2012) High latitude fish in a high CO2 world: Synergistic effects of elevated temperature and carbon dioxide on the metabolic rates of Antarctic notothenioids. Comp Biochem Physiol A 164: 154-161.
40. Strobel A, Bennecke S, Leo E, Mintenbeck K, Poertner HO, et al. (2012) Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front Zool 9: 28.
41. Sosinski J, S K, (1987) Biomass estimate of commercial fish on the shelf of South Georgia by the swept area method. Bull Sea Fish Inst 5-6: 8-14.
42. Duhamel G (1985) Distribution and abundance of fish on the Kerguelen Island shelf. Fifth Congress of European Icthyologists. Stockholm.
43. Casaux R, Mazzotta A, Barrera-Oro E, (1990) Seasonal aspects of the biology and diet of nearshore nototheniid fish at Potter Cove, South Shetland Islands, Antarctica. Polar Biol 11: 63-72.
44. Gon O, Heemstra P (1990) Fishes of the Southern Ocean. Grahamstown, South Africa: J.L.B. Smith Institute for Ichthyology. 462 p.
45. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel Program Developed for CO2 System Calculations. ORNL/CDIAC-105a ed. Oak Ridge, Tennessee Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.
46. Bradford M, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
47. Folch J, Lees M, Sloane Stanley GH, (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
48. Grim J, Miles D, Crockett E, (2010) Temperature acclimation alters oxidative capacities and composition of membrane lipids without influencing activities of enzymatic antioxidants or susceptibility to lipid peroxidation in fish muscle. J Exp Biol 213: 445-452.
49. Noack S (1980) Statistische Auswertung von Menue- und Versuchsdaten mit Taschenrechner und Tischcomputer: De Gruyter; 1980.
50. Efremov RG, Baradaran R, Sazanov LA, (2010) The architecture of respiratory complex I. Nature. 465: 441-445.
51. Brand MD, Harper ME, Taylor HC, (1993) Control of the effective P/O ratio of oxidative phosphorylation in liver mitochondria and hepatocytes. Biochem J 291: 739.
52. Poertner HO, Hardewig I, Peck LS, (1999) Mitochondrial Function and Critical Temperature in the Antarctic Bivalve, Laternula elliptica. Comp Biochem Physiol A 124: 179-189.
53. Johnston I, (2003) Muscle metabolism and growth in Antarctic fishes (suborder Notothenioidei): evolution in a cold environment. Comp Biochem Physiol B 136: 701-713.
54. Mark FC, Hirse T, Poertner HO, (2005) Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes. Polar Biol 28: 805-814.
55. Franklin CE, Davison W, Seebacher F, (2007) Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki. J Exp Biol 210: 3068-3074.
56. Robinson E, Davison W, (2008) The Antarctic notothenioid fish Pagothenia borchgrevinki is thermally flexible: acclimation changes oxygen consumption. Polar Biol 31: 317-326.
57. Trigari G, Pirini M, Ventrella V, Pagliarani A, Trombetti F, et al. (1992) Lipid composition and mitochondrial respiration in warm-and cold-adapted sea bass. Lipids 27: 371-377.
58. Wodtke E, (1981) Temperature adaptation of biological membranes: Compensation of the molar activity of cytochrome c oxidase in the mitochondrial energy-transducing membrane during thermal acclimation of the carp (Cyprinus carpio L.). Biochim Biophys Acta 640: 710-720.
59. Echtay KS, Esteves TC, Pakay JL, Jekabsons MB, Lambert AJ, et al. (2003) A signalling role for 4-hydroxy-2-nonenal in regulation of mitochondrial uncoupling. Embo J 22: 4103-4110.
60. Kamler E, Krasicka B, Rakusa-Suszczewski S, (2001) Comparison of lipid content and fatty acid composition in muscle and liver of two notothenioid fishes from Admiralty Bay (Antarctica): an eco-physiological perspective. Polar Biol 24: 735-743.
61. Hazel JR, (1972) The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L)-I. Properties of the enzyme and the effect of lipid extraction. Comp Biochem Physiol B 43: 837-861.
62. Guderley H, Johnston I, (1996) Plasticity of fish muscle mitochondria with thermal acclimation. J Exp Biol 199: 1311.
63. Poertner HO, (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213: 881-893.
64. Brauner CJ, Wang T, Wang Y, Richards JG, Gonzalez RJ, et al. (2004) Limited extracellular but complete intracellular acid-base regulation during short-term environmental hypercapnia in the armoured catfish, Liposarcus pardalis. J Exp Biol 207: 3381-3390.
65. Michaelidis B, Spring A, Poertner HO, (2007) Effects of long-term acclimation to environmental hypercapnia on extracellular acid-base status and metabolic capacity in Mediterranean fish Sparu saurata. Mar Biol 150: 1417-1429.
66. Deigweiher K, Hirse T, Bock C, Lucassen M, Poertner HO, (2010) Hypercapnia induced shifts in gill energy budgets of Antarctic notothenioids. J Comp Physiol B 180: 347-359.
67. Simpson DP, (1967) Regulation of renal citrate metabolism by bicarbonate ion and pH: observations in tissue slices and mitochondria. J Clin Investig 46: 225.
68. Poertner HO, (1987) Contributions of anaerobic metabolism to pH regulation in animal tissues: theory. J Exp Biol 131: 69-87.
69. Langenbuch M, Poertner HO, (2002) Changes in metabolic rate and N excretion in the marine invertebrate Sipunculus nudus under conditions of environmental hypercapnia: identifying effective acid-base variables. J Exp Biol 205: 1153-1160.
70. Robinson BH, Oei J, Cheema-Dhadli S, Halperin M, (1977) Regulation of citrate transport and pyruvate dehydrogenase in rat kidney cortex mitochondria by bicarbonate. J Biol Chem 252: 5661-5665.
71. Wanders RJA, Mejer AJ, Groen AK, Tager JM, (1983) Bicarbonate and the pathway of glutamate oxidation in isolated rat-liver mitochondria. Eur J Biochem 133: 245-254.
72. Mark FC, Lucassen M, Poertner HO, (2006) Thermal sensitivity of uncoupling protein expression in polar and temperate fish. Comp Biochem Physiol D 1: 365-374.