Mitochondrial thermo-sensitivity in invasive and native freshwater mussels

Abstract

Climate change is impacting many, if not all, forms of life. Increases in extreme temperature fluctuations and average temperatures can cause stress, particularly in aquatic sessile ectotherms such as freshwater mussels. However, some species seem to thrive more than others in face of temperature-related stressors. Thermal tolerance may for example explain invasive species success. It is also known that mitochondria can play a key role in setting an ectothermic species’ thermal tolerance. In this study, we aimed to characterize the mitochondrial thermo-tolerance in invasive and endemic freshwater mussels. With the use of high-resolution respirometry, we analyzed the mitochondrial respiration of two freshwater bivalve species exposed to a broad range of temperatures. We noticed that the invasive dreissenid Dreissena bugensis possessed a less thermo-tolerant mitochondrial metabolism than the endemic unionid Elliptio complanata. This lack of tolerance was linked with a more noticeable aerobic metabolic depression at elevated temperatures. This decrease in mitochondrial metabolic activity was also linked with an increase in leak oxygen consumption as well as a stable maintenance of the activity of cytochrome c oxidase in both species. These findings may be associated both with species’ life history characteristics, as D. bugensis is more adapted to unstable habitats, in which selection pressures for resistance adaptations are reduced. Our findings add to the growing body of literature characterizing the mitochondrial metabolism of many aquatic ectotherms in our changing world.

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

“…However, the literature is ambiguous on the potential limitation of CS (and PDH) on ectotherm metabolism at high temperatures and it has been disputed in mussels (Hraoui et al, 2020).…”

“…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).…”

Flexible Thermal Sensitivity of Mitochondrial Oxygen Consumption and Substrate Oxidation in Flying Insect Species

“…At the cellular level, this implies that mitochondria have to adjust their oxygen consumption to supply the amount of ATP required to match this increased metabolic demand and restore homeostasis when temperature increases. Therefore, mitochondrial thermal sensitivity has been put forward to tentatively explain organismal failure at high temperatures and is believed to be paramount for thermal adaptation of several organisms ( Fangue et al, 2009 ; Iftikar et al, 2014 ; Chung et al, 2018 ; Harada et al, 2019 ; Pichaud et al, 2019 ; Hraoui et al, 2020 ; Hraoui et al, 2021 ). However, the study of insects has often been overlooked mainly due to technical reasons which resulted in a gap of knowledge concerning mitochondrial functions and the implication of mitochondrial adaptation in insects at high temperature [but see ( Davison and Bowler, 1971 ; Kashmerry and Bowler, 1977 ; Chamberlin, 2004 ; Pichaud et al, 2010 ; Pichaud et al, 2011 ; Pichaud et al, 2012 ; Pichaud et al, 2013 ; Jørgensen et al, 2021 )].…”

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

“…Heart CS (and PDH) activity was found to decrease at temperatures around and exceeding CT max in European perch ( Perca fluviatilis ), which was interpreted as an impaired capacity to oxidize pyruvate which could ultimately limit the entry of electrons into the ETS (Ekström et al, 2017). However, the literature is ambiguous on the potential limitation of CS (and PDH) on ectotherm metabolism at high temperatures and it has been disputed in mussels (Hraoui et al, 2020). Nevertheless, it must be noted that the enzymatic activities measured in vitro here represent the maximal catalytic capacity and that they may not directly reflect metabolic flux in vivo .…”

“…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).…”