Advertisement

Journal of Comparative Physiology B

, Volume 184, Issue 8, pp 991–1001 | Cite as

Thermal plasticity of skeletal muscle mitochondrial activity and whole animal respiration in a common intertidal triplefin fish, Forsterygion lapillum (Family: Tripterygiidae)

  • J. R. Khan
  • F. I. Iftikar
  • N. A. Herbert
  • Erich Gnaiger
  • A. J. R. HickeyEmail author
Original Paper

Abstract

Oxygen demand generally increases in ectotherms as temperature rises in order to sustain oxidative phosphorylation by mitochondria. The thermal plasticity of ectotherm metabolism, such as that of fishes, dictates a species survival and is of importance to understand within an era of warming climates. Within this study the whole animal O2 consumption rate of a common New Zealand intertidal triplefin fish, Forsterygion lapillum, was investigated at different acclimation temperatures (15, 18, 21, 24 or 25 °C) as a commonly used indicator of metabolic performance. In addition, the mitochondria within permeabilised skeletal muscle fibres of fish acclimated to a moderate temperature (18 °C Cool acclimation group—CA) and a warm temperature (24 °C. Warm acclimation group—WA) were also tested at 18, 24 and 25 °C in different states of coupling and with different substrates. These two levels of analysis were carried out to test whether any peak in whole animal metabolism reflected the respiratory performance of mitochondria from skeletal muscle representing the bulk of metabolic tissue. While standard metabolic rate (SMR- an indicator of total maintenance metabolism) and maximal metabolic rate (\(\dot{M}\)O2 max) both generally increased with temperature, aerobic metabolic scope (AMS) was maximal at 24 °C, giving the impression that whole animal (metabolic) performance was optimised at a surprisingly high temperature. Mitochondrial oxygen flux also increased with increasing assay temperature but WA fish showed a lowered response to temperature in high flux states, such as those of oxidative phosphorylation and in chemically uncoupled states of respiration. The thermal stability of mitochondria from WA fish was also noticeably greater than CA fish at 25 °C. However, the predicted contribution of respirational flux to ATP synthesis remained the same in both groups and WA fish showed higher anaerobic activity as a result of high muscle lactate loads in both rested and exhausted states. CA fish had a comparably lower level of resting lactate and took 30 % longer to fatigue than WA fish. Despite some apparent acclimation capacity of skeletal muscle mitochondria, the ATP synthesis capacity of this species is constrained at high temperatures, and that a greater fraction of metabolism in skeletal muscle appears to be supported anaerobically at higher temperatures. The AMS peak at 24 °C does not therefore represent utilisation efficiency of oxygen but, rather, the temperature where scope for oxygen flow is greatest.  

Keywords

Mitochondria Temperature acclimation Electron transport system Lactate Anerobic metabolism 

References

  1. Bouchard P, Guderley H (2003) Time course of the response of mitochondria from oxidative muscle during thermal acclimation of rainbow trout, Oncorhynchus mykiss. J Exp Biol 206:3455–3465PubMedCrossRefGoogle Scholar
  2. Brand MD (1990) The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate. J Theor Biol 145:267–286PubMedCrossRefGoogle Scholar
  3. Brand MD (2005) The efficiency and plasticity of mitochondrial energy transduction. Biochem Soc Trans 33:897–904PubMedCrossRefGoogle Scholar
  4. Brown GC (1999) Nitric oxide and mitochondrial respiration. Biochim Biophys Acta 1411:351–369PubMedCrossRefGoogle Scholar
  5. Clark TD, Jeffries KM, Hinch SG, Farrell AP (2011) Exceptional aerobic scope and cardiovascular performance of pink salmon (Oncorhynchus gorbuscha) may underlie resilience in a warming climate. J Exp Biol 214:3074–3081PubMedCrossRefGoogle Scholar
  6. Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216:2771–2782PubMedCrossRefGoogle Scholar
  7. Condon CH, Chenoweth SF, Wilson RS (2010) Zebrafish take their cue from temperature but not photoperiod for the seasonal plasticity of thermal performance. J Exp Biol 213:3705–3709PubMedCrossRefGoogle Scholar
  8. Dupont-Prinet A, Vagner M, Chabot D, Audet C (2013) Impact of hypoxia on the metabolism of Greenland halibut (Reinhardtius hippoglossoides). Can J Fisheries Aquat Sci 70:461–469CrossRefGoogle Scholar
  9. Farrell AP (2002) Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes. Comp Biochem Physiol 132A:797–810CrossRefGoogle Scholar
  10. Franklin CE, Farrell AP, Altimiras J, Axelsson M (2013) Thermal dependence of cardiac function in arctic fish: implications of a warming world. J Exp Biol 216:4251–4255PubMedCrossRefGoogle Scholar
  11. Fry FEG (1971) The effect on environmental factors on the physiology of fish. In: Hoar WS, Randall DJ (eds) Fish physiology, 4th edn. Academic Press, New York, pp 1–98Google Scholar
  12. Galli GLJ, Richards JG (2012) The effect of temperature onmitochondrial respirationin permeabilized cardiac fibres from the fresh water turtle, Trachemys scripta. J Therm Biol 37:195–200CrossRefGoogle Scholar
  13. Gnaiger E (2008) Mitochondrial pathways through complexes I + II: convergent electron transport at the Q-junction and additive effect of substrate combinations. In: Gnaiger E (ed) Mitochondrial pathways and respiratory control, 2nd edn. MiPNet Publications, Innsbruck, pp 21–37Google Scholar
  14. Gnaiger E (2011) Mitochondrial pathways through Complexes I + II: convergent electron transport at the Q-junction and additive effect of substrate combinations. Oroboros Instruments, Mitochondrial Physiology NetworkGoogle Scholar
  15. 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 205:2237–2249PubMedGoogle Scholar
  16. Hammill E, Wilson RS, Johnston IA (2004) Sustained swimming performance and muscle structure are altered by thermal acclimation in male mosquitofish. J Therm Biol 29:251–257CrossRefGoogle Scholar
  17. Healy TM, Schulte PM (2012) Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus). Physiol Biochem Zool 85:107–119PubMedCrossRefGoogle Scholar
  18. Hickey AJ, Clements KD (2003) Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison. J Comp Physiol B 173:113–123PubMedGoogle Scholar
  19. Hilton Z, Clements K, Hickey A (2010) Temperature sensitivity of cardiac mitochondria in intertidal and subtidal triplefin fishes. J Comp Physiol B 180:1–12CrossRefGoogle Scholar
  20. Iftikar FI, Hickey AJR (2013) Do mitochondria limit hot fish hearts? Understanding the role of mitochondrial function with heat stress in Notolabrus celidotus. PLoS ONE 8:e64120PubMedCentralPubMedCrossRefGoogle Scholar
  21. 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 Biol Ecol 395:232–239CrossRefGoogle Scholar
  22. Iftikar FI, MacDonald JR, Baker DW, Renshaw GMC, Hickey AJR (2014a) Could thermal sensitivity of mitochondria determine species distributions in a changing climate? J Exp Biol 217:2348–2357PubMedCrossRefGoogle Scholar
  23. Iftikar FI, MacDonald JR, Baker DW, Renshaw GMC, Hickey AJR (2014) Could thermal sensitivity of mitochondria determine species distributions in a changing climate? J Exp Biol (in press)Google Scholar
  24. Johnston I, Lucking M (1978) Temperature induced variation in the distribution of different types of muscle fibre in the goldfish (Carassius auratus). J Comp Physiol 124:111–116CrossRefGoogle Scholar
  25. Khan JR, Herbert NA (2012) The behavioural thermal preference of the common triplefin (Forsterygion lapillum) tracks aerobic scope optima at the upper thermal limit of its distribution. J Therm Biol 37:118–124CrossRefGoogle Scholar
  26. Newsholme EA, Crabtree B (1986) Maximum catalytic activity of some key enzymes in provision of physiological useful information about metabolic fluxes. J Exp Zool 239: 159–163PubMedCrossRefGoogle Scholar
  27. Parks RE, Adler J, Copenhaver JH (1955) The efficiency of oxidative phosphorylation in mitochondria from diabetic rats. J Biol Chem 214:693–698PubMedGoogle Scholar
  28. Pesta D, Gnaiger E (2012) High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. In: Palmeira CM, Moreno AJ (eds) Mitochondrial bioenergetics. Humana Press, New York, pp 25–58CrossRefGoogle Scholar
  29. Picard M, Taivassalo T, Gouspillou G, Hepple RT (2011) Mitochondria: isolation, structure and function. J PhysiolGoogle Scholar
  30. Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol 132A:739–761CrossRefGoogle Scholar
  31. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315Google Scholar
  32. Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Resp Physiol Neurobiol 141:243–260CrossRefGoogle Scholar
  33. Reidy SP, Nelson JA, Tang Y, Kerr SR (1995) Post-exercise metabolic rate in Atlantic cod and its dependence upon the method of exhaustion. J Fish Biol 477:377–386CrossRefGoogle Scholar
  34. Richter A, Kolmes SA (2005) Maximum temperature limits for chinook, coho, and chum salmon, and steelhead trout in the Pacific northwest. Rev Fisheries Sci 13:23–49CrossRefGoogle Scholar
  35. Seebacher F, Brand MD, Else PL, Guderley H, Hulbert AJ, Moyes CD (2010) Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiol Biochem Zool 83:721–732PubMedCrossRefGoogle Scholar
  36. St-Pierre J, Charest PM, Guderley H (1998) Relative contribution of quantitative and qualitative changes in mitochondria to metabolic compensation during seasonal acclimatisation of rainbow trout Oncorhynchus mykiss. J Exp Biol 201:2961–2970Google Scholar
  37. Veksler VI, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA (1987) Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892:191–196PubMedCrossRefGoogle Scholar
  38. Wilson RS, Condon CHL, Johnston IA (2007) Consequences of thermal acclimation for the mating behaviour and swimming performance of female mosquito fish. Philos Trans R Soc B 362:2131–2139CrossRefGoogle Scholar
  39. Zukiene R, Nauciene Z, Ciapaite J, Mildaziene V (2010) Acute temperature resistance threshold in heart mitochondria: febrile temperature activates function but exceeding it collapses the membrane barrier. Int J Hyperthermia 26:56–66PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • J. R. Khan
    • 1
  • F. I. Iftikar
    • 2
  • N. A. Herbert
    • 1
  • Erich Gnaiger
    • 3
  • A. J. R. Hickey
    • 2
    Email author
  1. 1.Institute of Marine Science, Leigh Marine LaboratoryUniversity of AucklandWarkworthNew Zealand
  2. 2.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  3. 3.D. Swarovski Research Laboratory, Department of General and Transplant SurgeryMedical University of InnsbruckInnsbruckAustria

Personalised recommendations