Physiological performance of warm-adapted marine ectotherms: Thermal limits of mitochondrial energy transduction efficiency

Abstract

Thermal regimes in aquatic systems have profound implications for the physiology of ectotherms. In particular, the effect of elevated temperatures on mitochondrial energy transduction in tropical and subtropical teleosts may have profound consequences on organismal performance and population viability. Upper and lower whole-organism critical temperatures for teleosts suggest that subtropical and tropical species are not susceptible to the warming trends associated with climate change, but sub-lethal effects on energy transduction efficiency and population dynamics remain unclear. The goal of the present study was to compare the thermal sensitivity of processes associated with mitochondrial energy transduction in liver mitochondria from the striped mojarra (Eugerres plumieri), the whitemouth croaker (Micropogonias furnieri) and the palometa (Trachinotus goodei), to those of the subtropical pinfish (Lagodon rhomboides) and the blue runner (Caranx crysos). Mitochondrial function was assayed at temperatures ranging from 10 to 40°C and results obtained for both tropical and subtropical species showed a reduction in the energy transduction efficiency of the oxidative phosphorylation (OXPHOS) system in most species studied at temperatures below whole-organism critical temperature thresholds. Our results show a loss of coupling between O2 consumption and ATP production before the onset of the critical thermal maxima, indicating that elevated temperature may severely impact the yield of ATP production per carbon unit oxidized. As warming trends are projected for tropical regions, increasing water temperatures in tropical estuaries and coral reefs could impact long-term growth and reproductive performance in tropical organisms, which are already close to their upper thermal limit.

Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study usingDrosophila

“…CI-supported) OCRs measured in in vivo heat-treated blowflies was reduced by 50 % compared to non-heated controls (El-Wadawi and Bowler, 1996). Complex I has also been suggested to be a primary site of heat failure in liver mitochondria from marine fishes (Chung et al, 2018;Martinez et al, 2016), in marine crustaceans (Iftikar et al, 2010), as well as in maize (Pobezhimova et al, 1996). In the present study the OXPHOS coupling efficiency j≈P (the linearized form of the respiratory control ratio, RCR) at the level of complex I, decreased with higher temperature (Table 1), which is an obvious consequence of the hyperthermic decrease in CI-OXPHOS rather than an increase in CI-LEAK, as previously observed (Hilton et al, 2010;Iftikar et al, 2010;Iftikar et al, 2014;Lemieux et al, 2010b).…”

“…Metabolic demand increases with temperature and to maintain cellular homeostasis the rate of mitochondrial aerobic respiration must keep pace (Blier et al, 2014;Schulte, 2015). Accordingly, thermal sensitivity of mitochondria has been suggested to be important for thermal tolerance and thermal adaptations of mitochondrial functions have been observed in several ectothermic phyla (Chung et al, 2018;Ekström et al, 2017;Fangue et al, 2009;Harada et al, 2019;Havird et al, 2020;Hraoui et al, 2020;Hunter-Manseau et al, 2019;Iftikar et al, 2010;Iftikar et al, 2014;Kake-Guena et al, 2017;Martinez et al, 2016, see also Chung and Schulte, 2020). Most mitochondrial studies addressing the effects of high temperature in ectotherms have focused on aquatic invertebrates or fish, while only a few studies have used insects, even though they comprise > 70% of all animal species (Stork, 2018) and have the most rapidly contracting muscles in nature (Beenakkers et al, 1984;Candy et al, 1997) (but see Chamberlin (2004), Pichaud et al (2010;2011; and references below for studies on insect mitochondrial function).…”

Reduced Mitochondrial Efficiency Explains Mismatched Growth and Metabolic Rate at Supraoptimal Temperatures

“…Although the mechanisms of temperature-induced physiological costs are likely multifaceted (e.g., ATP-dependent changes in gene expression, upregulation of protein repair mechanisms; Somero 2011), it seems clear that the efficiency with which the mitochondria convert consumed oxygen into ATP plays a major role. This mitochondrial efficiency hypothesis (MEH) rests on two well-established observations: (i) the coupling efficiency between oxygen consumption and ATP production in mitochondria (the respiratory control ratio [RCR]) is temperature dependent (Weinstein and Somero 1998;Hardewig et al 1999;Martinez et al 2013Martinez et al , 2016 and (ii) non-ATP-producing respiration (LEAK) represents a significant fraction of the cost of maintaining an organism and dramatically increases at supraoptimal temperatures in ectotherms (Hardewig et al 1999;Abele et al 2002;Chamberlin 2004;Martinez et al 2013). Thus, the MEH hypothesizes that reduced mitochondrial energy transduction efficiency, due to increased protonleak respiration, is a key mechanism driving whole-organism performance.…”

Dramatic changes in mitochondrial substrate use at critically high temperatures: a comparative study usingDrosophila

“…CI-supported) OCRs measured in in vivo heat-treated blowflies was reduced by 50 % compared to non-heated controls (El-Wadawi and Bowler, 1996). Complex I has also been suggested to be a primary site of heat failure in liver mitochondria from marine fishes (Chung et al, 2018; Martinez et al, 2016), in marine crustaceans (Iftikar et al, 2010), as well as in maize (Pobezhimova et al, 1996). In the present study the OXPHOS coupling efficiency j≈P (the linearized form of the respiratory control ratio, RCR) at the level of complex I, decreased with higher temperature (Table 1), which is an obvious consequence of the hyperthermic decrease in CI-OXPHOS rather than an increase in CI-LEAK, as previously observed (Hilton et al, 2010; Iftikar et al, 2010; Iftikar et al, 2014; Lemieux et al, 2010b).…”

“…Metabolic demand increases with temperature and to maintain cellular homeostasis the rate of mitochondrial aerobic respiration must keep pace (Blier et al, 2014; Schulte, 2015). Accordingly, thermal sensitivity of mitochondria has been suggested to be important for thermal tolerance and thermal adaptations of mitochondrial functions have been observed in several ectothermic phyla (Chung et al, 2018; Ekström et al, 2017; Fangue et al, 2009; Harada et al, 2019; Havird et al, 2020; Hraoui et al, 2020; Hunter-Manseau et al, 2019; Iftikar et al, 2010; Iftikar et al, 2014; Kake-Guena et al, 2017; Martinez et al, 2016, see also Chung and Schulte, 2020). Most mitochondrial studies addressing the effects of high temperature in ectotherms have focused on aquatic invertebrates or fish, while only a few studies have used insects, even though they comprise > 70% of all animal species (Stork, 2018) and have the most rapidly contracting muscles in nature (Beenakkers et al, 1984; Candy et al, 1997) (but see Chamberlin (2004), Pichaud et al (2010; 2011; 2012; 2013) and references below for studies on insect mitochondrial function).…”