Could thermal sensitivity of mitochondria determine species distribution in a changing climate?

Abstract

For many aquatic species, the upper thermal limit (T max ) and the heart failure temperature (T HF ) are only a few degrees away from the species' current environmental temperatures. While the mechanisms mediating temperature-induced heart failure (HF) remain unresolved, energy flow and/or oxygen supply disruptions to cardiac mitochondria may be impacted by heat stress. Recent work using a New Zealand wrasse (Notolabrus celidotus) found that ATP synthesis capacity of cardiac mitochondria collapses prior to T HF . However, whether this effect is limited to one species from one thermal habitat remains unknown. The present study confirmed that cardiac mitochondrial dysfunction contributes to heat stress-induced HF in two additional wrasses that occupy cold temperate (Notolabrus fucicola) and tropical (Thalassoma lunare) habitats. With exposure to heat stress, T. lunare had the least scope to maintain heart function with increasing temperature. Heat-exposed fish of all species showed elevated plasma succinate, and the heart mitochondria from the cold temperate N. fucicola showed decreased phosphorylation efficiencies (depressed respiratory control ratio, RCR), cytochrome c oxidase (CCO) flux and electron transport system (ETS) flux. In situ assays conducted across a range of temperatures using naive tissues showed depressed complex II (CII) and CCO capacity, limited ETS reserve capacities and lowered efficiencies of pyruvate uptake in T. lunare and N. celidotus. Notably, alterations of mitochondrial function were detectable at saturating oxygen levels, indicating that cardiac mitochondrial insufficiency can occur prior to HF without oxygen limitation. Our data support the view that species distribution may be related to the thermal limits of mitochondrial stability and function, which will be important as oceans continue to warm.

The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment

“…There have been some measurements of the effects of temperature on aerobic metabolism at the cellular level in animals (Somero and DeVries, 1967;Hoskins and Aleksiuk, 1973;Jorjani and Ozturk, 1999) and some data sets conform well to the Arrhenius equation and others do not. Similar patterns occur for measurements of oxygen consumption by isolated mitochondria (van den Thillart and Modderkolk, 1978;Somero et al, 1996;Weinstein and Somero, 1998;Hardewig et al, 1999;Abele et al, 2002;Somero, 2002;Johnston et al, 1994;Fangue et al, 2009;Hilton et al, 2010;Iftikar et al, 2010Iftikar et al, , 2014Iftikar and Hickey, 2013). For example, Fig.…”

“…Proton leak allows protons to move across the mitochondrial inner membrane via pathways other than the ATP synthase, thus dissipating the proton motive force and driving oxygen consumption without generating ATP. Substantial amounts of data suggest that the thermal sensitivities of ATP generation and proton leak differ (Hardewig et al, 1999;Hilton et al, 2010;Iftikar et al, 2010Iftikar et al, , 2014Iftikar and Hickey, 2013) because of increases in proton permeability due to changes in membrane fluidity at higher temperatures (Seebacher et al, 2010;Zukiene et al, 2010). As a result, proton leak represents an increasing fraction of oxygen consumption as temperature rises (Hilton et al, 2010;Seebacher et al, 2010;Iftikar and Hickey, 2013) causing reductions in the efficiency of mitochondrial ATP production with increasing temperature.…”

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

“…Two different ratios were calculated to evaluate the functionality and the quality of the mitochondrial preparations used in the experiment: (i) the P/L ratio (CI-OXPHOS/CI-LEAK), which is usually taken as a good indicator of mitochondrial quality and of mitochondrial coupling (Gnaiger, 2009;Iftikar et al, 2014); and (ii) the cytochrome c effect (CIc-OXPHOS/CI-OXPHOS) to evaluate the structural integrity of the outer mitochondrial membrane (Kuznetsov et al, 2008).…”

“…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).…”

“…Even so, it was recently shown that the cardiac tissue of Silurus meridionalis displayed metabolic over-compensation with seasonal acclimatization, compared with other tissues (Yan and Xie, 2015). In fact, it has recently been suggested that thermal sensitivity of cardiac mitochondrial metabolism might be the very parameter determining species distribution during warming (Iftikar et al, 2014).…”