Literature DB >> 25269418

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

J R Khan1, F I Iftikar, N A Herbert, Erich Gnaiger, A J R Hickey.   

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 ([Formula: see text]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.

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Year:  2014        PMID: 25269418     DOI: 10.1007/s00360-014-0861-9

Source DB:  PubMed          Journal:  J Comp Physiol B        ISSN: 0174-1578            Impact factor:   2.200


  26 in total

Review 1.  Cardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes.

Authors:  A P Farrell
Journal:  Comp Biochem Physiol A Mol Integr Physiol       Date:  2002-08       Impact factor: 2.320

2.  The contribution of the leak of protons across the mitochondrial inner membrane to standard metabolic rate.

Authors:  M D Brand
Journal:  J Theor Biol       Date:  1990-07-24       Impact factor: 2.691

3.  Key metabolic enzymes and muscle structure in triplefin fishes (Tripterygiidae): a phylogenetic comparison.

Authors:  A J R Hickey; K D Clements
Journal:  J Comp Physiol B       Date:  2003-02-07       Impact factor: 2.200

4.  Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus).

Authors:  Timothy M Healy; Patricia M Schulte
Journal:  Physiol Biochem Zool       Date:  2012-02-01       Impact factor: 2.247

5.  Zebrafish take their cue from temperature but not photoperiod for the seasonal plasticity of thermal performance.

Authors:  Catriona H Condon; Stephen F Chenoweth; Robbie S Wilson
Journal:  J Exp Biol       Date:  2010-11-01       Impact factor: 3.312

6.  Time course of the response of mitochondria from oxidative muscle during thermal acclimation of rainbow trout, Oncorhynchus mykiss.

Authors:  Patrice Bouchard; Helga Guderley
Journal:  J Exp Biol       Date:  2003-10       Impact factor: 3.312

Review 7.  Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals.

Authors:  H O Pörtner
Journal:  Comp Biochem Physiol A Mol Integr Physiol       Date:  2002-08       Impact factor: 2.320

Review 8.  Oxygen limited thermal tolerance in fish?--Answers obtained by nuclear magnetic resonance techniques.

Authors:  H O Pörtner; F C Mark; C Bock
Journal:  Respir Physiol Neurobiol       Date:  2004-08-12       Impact factor: 1.931

9.  Thermal dependence of cardiac function in arctic fish: implications of a warming world.

Authors:  Craig E Franklin; Anthony P Farrell; Jordi Altimiras; Michael Axelsson
Journal:  J Exp Biol       Date:  2013-08-15       Impact factor: 3.312

10.  Do mitochondria limit hot fish hearts? Understanding the role of mitochondrial function with heat stress in Notolabrus celidotus.

Authors:  Fathima I Iftikar; Anthony J R Hickey
Journal:  PLoS One       Date:  2013-05-28       Impact factor: 3.240

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  12 in total

1.  Intertidal triplefin fishes have a lower critical oxygen tension (Pcrit), higher maximal aerobic capacity, and higher tissue glycogen stores than their subtidal counterparts.

Authors:  Tristan J McArley; Anthony J R Hickey; Lisa Wallace; Andreas Kunzmann; Neill A Herbert
Journal:  J Comp Physiol B       Date:  2019-04-02       Impact factor: 2.200

2.  Warm acclimation alters antioxidant defences but not metabolic capacities in the Antarctic fish, Notothenia coriiceps.

Authors:  Kristin M O'Brien; Corey A Oldham; Jon Sarrimanolis; Autumn Fish; Luke Castellini; Jenna Vance; Hayley Lekanof; Elizabeth L Crockett
Journal:  Conserv Physiol       Date:  2022-08-02       Impact factor: 3.252

3.  Energetic, antioxidant, inflammatory and cell death responses in the red muscle of thermally stressed Sparus aurata.

Authors:  Konstantinos Feidantsis; Ioannis Georgoulis; Andreas Zachariou; Berrin Campaz; Marilena Christoforou; Hans O Pörtner; Basile Michaelidis
Journal:  J Comp Physiol B       Date:  2020-04-25       Impact factor: 2.200

4.  Post-hatching development of mitochondrial function, organ mass and metabolic rate in two ectotherms, the American alligator (Alligator mississippiensis) and the common snapping turtle (Chelydra serpentina).

Authors:  Sarah K G Sirsat; Tushar S Sirsat; Edwin R Price; Edward M Dzialowski
Journal:  Biol Open       Date:  2016-04-15       Impact factor: 2.422

5.  Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction.

Authors:  Sjannie Lefevre
Journal:  Conserv Physiol       Date:  2016-03-23       Impact factor: 3.079

6.  Remodeling pathway control of mitochondrial respiratory capacity by temperature in mouse heart: electron flow through the Q-junction in permeabilized fibers.

Authors:  Hélène Lemieux; Pierre U Blier; Erich Gnaiger
Journal:  Sci Rep       Date:  2017-06-06       Impact factor: 4.379

7.  Low oxygen levels can help to prevent the detrimental effect of acute warming on mitochondrial efficiency in fish.

Authors:  Elisa Thoral; Damien Roussel; Christos Chinopoulos; Loïc Teulier; Karine Salin
Journal:  Biol Lett       Date:  2021-02-10       Impact factor: 3.703

8.  Thermally tolerant intertidal triplefin fish (Tripterygiidae) sustain ATP dynamics better than subtidal species under acute heat stress.

Authors:  Jaime R Willis; Anthony J R Hickey; Jules B L Devaux
Journal:  Sci Rep       Date:  2021-05-26       Impact factor: 4.379

9.  Diet and temperature modify the relationship between energy use and ATP production to influence behavior in zebrafish (Danio rerio).

Authors:  Amélie Le Roy; Geoffrey P F Mazué; Neil B Metcalfe; Frank Seebacher
Journal:  Ecol Evol       Date:  2021-06-21       Impact factor: 2.912

10.  Mismatched light and temperature cues disrupt locomotion and energetics via thyroid-dependent mechanisms.

Authors:  Amélie Le Roy; Frank Seebacher
Journal:  Conserv Physiol       Date:  2020-06-11       Impact factor: 3.079

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