Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins,phospholipids and their fatty acid compositions

Abstract

International audienceChanges in the properties of mitochondria from oxidative muscle of rainbow trout Oncorhynchus mykiss were examined during warm (5 degrees C to 15 degrees C) acclimation. Trout were studied shortly after the initial thermal change and after 8 weeks acclimation to 15 degrees C. To identify potential mechanisms by which oxidative capacities change, the modifications of phospholipid composition, membrane proteins and functional capacities of red muscle mitochondria were examined. Marked functional changes of isolated muscle mitochondria during warm acclimation of rainbow trout were reflected by a host of modifications in phospholipid composition, but by few shifts in protein components. Shortly after transfer of trout from 5 degrees C to 15 degrees C, the maximal oxidative capacity of mitochondria measured at 15 degrees C increased slightly, but rates at both assay temperatures (5 degrees C and 15 degrees C) decreased markedly after warm acclimation. The increase in capacity in short-term warm exposed trout was most pronounced when rates at 15 degrees C were expressed relative to cytochrome a and c(1) levels. Non-phosphorylating (State 4) rates of oxygen uptake increased with short-term warm exposure before returning to initial levels after warm acclimation. Cytochrome c oxidase (CCO) activity in the mitochondrial preparations decreased with warm acclimation. The thermal sensitivity of the ADP affinity was markedly modified during short-term warm exposure, when the ADP/O ratio increased, but warm acclimation returned these values to those observed initially. ADP affinity increased after warm acclimation. Changes in the mitochondrial content of cytochromes and adenine nucleotide translocase (ANT) could not explain these patterns. On the other hand, changes in the proportions of the lipid classes and in the acyl chain composition of certain phospholipid classes mirror the modifications in functional properties. Short-term exposure to 15 degrees C decreased the ratio of diacylphosphatidylethanolamine/diacylphosphatidylcholine (diacylPE/diacylPC), whereas warm acclimation led to restructuring of fatty acids (FA) and to increases of plasmalogen forms of PE and PC. Modification of overall membrane unsaturation did not appear to be the primary aim of restructuring membrane FA during warm acclimation, as total mitochondrial phospholipids and the major phospholipid classes only showed slight shifts of their acyl composition with warm acclimation. On the other hand, natural lysophosphatidylcholine (LysoPC) showed dramatic changes in FA content, as 16:0 and 18:1n-9 doubled whereas 22:6n-3 decreased from around 50% to 32% in warm acclimated trout. Similarly, in cardiolipin (CL), the levels of 16:0 and 18:1n-7 halved while 18:2n-6 increased to over 20% of the FA with warm acclimation. Given the central role of CL in modulating the activity of CCO, F(0)F(1)-ATPase and ANT, these changes suggest that specific compositional changes in CL are important modulators of mitochondrial capacities. The many structural ...

Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus)

“…Low-temperature acclimation is associated with increased mitochondrial oxidative phosphorylation (OXPHOS) capacity, mitochondrial volume density and alterations in mitochondrial membrane composition (Chung and Schulte, 2015;Egginton and Johnston, 1984;Grim et al, 2010;Fangue et al, 2009;Kraffe et al, 2007;Dhillon and Schulte, 2011;Schnell and Seebacher, 2008). In contrast, hightemperature acclimation has been associated with changes in mitochondrial membrane fatty acid saturation and lowered mitochondrial respiratory capacity (Chung and Schulte, 2015;Guderley and Johnston, 1996;Khan et al, 2014;Strobel et al, 2013;Baris et al, 2016a;Fangue et al, 2009).…”

Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

“…This is principally due to decreased activation energy of enzymatic reactions, and an increased probability of interaction between enzymes and substrates (Aledo et al, 2010). Moreover, the fluidity of mitochondrial membranes increases during the initial stage of warming due to modifications of phospholipid composition (Hazel and Landrey, 1988a,b;Hazel, 1995;Kraffe et al, 2007). This can influence the capacity of membrane-bound enzymes, such as the complexes of the electron transport system (ETS) that depend on the physical state of the lipid environment in which they function (Kraffe et al, 2007;Martin et al, 2013).…”

“…Moreover, the fluidity of mitochondrial membranes increases during the initial stage of warming due to modifications of phospholipid composition (Hazel and Landrey, 1988a,b;Hazel, 1995;Kraffe et al, 2007). This can influence the capacity of membrane-bound enzymes, such as the complexes of the electron transport system (ETS) that depend on the physical state of the lipid environment in which they function (Kraffe et al, 2007;Martin et al, 2013). Acute warming can also result in adverse effects subsequent to increased mitochondrial functions, such as unsustainable oxygen consumption and increased production of reactive oxygen species (Abele et al, 2002;Chung and Schulte, 2015).…”

“…Acute warming can also result in adverse effects subsequent to increased mitochondrial functions, such as unsustainable oxygen consumption and increased production of reactive oxygen species (Abele et al, 2002;Chung and Schulte, 2015). However, during warm acclimation for several weeks, decreases in the rates of mitochondrial oxygen consumption and enzyme catalytic capacities, as well as adjustments of membrane architecture via changes in phospholipid proportions and fatty acid composition are typically observed, probably to limit these adverse effects (Hochachka and Somero, 1973;Hazel and Landrey, 1988a,b;Guderley and Johnston, 1996;Guderley and St-Pierre, 2002;Kraffe et al, 2007;Fangue et al, 2009;Chung and Schulte, 2015). Nonetheless, a shortcoming of most laboratory acclimation experiments is that only 'snapshots' of information are obtained (e.g.…”

“…Moreover, due to the complexity of the thermal acclimation process, the different components of mitochondrial metabolism affected by temperature are not clear, as they may depend on the time course and the intensity of the thermal exposure (Hazel, 1972(Hazel, , 1995Sidell, 1983;Blier and Guderley, 1993;St-Pierre et al, 1998;Guderley, 2004;Itoi et al, 2003;Kraffe et al, 2007;Iftikar et al, 2014;Jayasundara et al, 2015). For example, in isolated mitochondria from the red muscle of rainbow trout, Oncorhynchus mykiss, a temperature increase from 5 to 9°C over 2 days (Bouchard and Guderley, 2003) or from 5 to 15°C over 3 days (Kraffe et al, 2007) did not significantly change rates of pyruvate oxidation (state 3 and state 4; oxygen consumption in presence and absence of ADP, respectively, when pyruvate is provided to the mitochondria).…”