Mitochondrial Adaptations to Variable Environments and Their Role in Animals’ Stress Tolerance

Mitochondria are the key organelles involved in energy and redox homeostasis, cellular signaling, and survival. Animal mitochondria are exquisitely sensitive to environmental stress, and stress-induced changes in the mitochondrial integrity and function have major consequences for the organismal performance and fitness. Studies in the model organisms such as terrestrial mammals and insects showed that mitochondrial dysfunction is a major cause of injury during pathological conditions and environmental insults such as hypoxia, ischemia-reperfusion, and exposure to toxins. However, animals from highly stressful environments (such as the intertidal zone of the ocean) can maintain mitochondrial integrity and function despite intense and rapid fluctuations in abiotic conditions and associated changes in the intracellular milieu. Recent studies demonstrate that mitochondria of intertidal organisms (including mollusks, crustaceans, and fish) are capable of maintaining activity of mitochondrial electron transport system (ETS), ATP synthesis, and mitochondrial coupling in a broad range of temperature, osmolarity, and ion content. Mitochondria of intertidal organisms such as mollusks are also resistant to hypoxia-reoxygenation injury and show stability or even upregulation of the mitochondrial ETS activity and ATP synthesis capacity during intermittent hypoxia. In contrast, pH optima for mitochondrial ATP synthesis and respiration are relatively narrow in intertidal mollusks and may reflect adaptation to suppress metabolic rate during pH shifts caused by extreme stress. Sensitivity to anthropogenic pollutants (such as trace metals) in intertidal mollusks appears similar to that of other organisms (including mammals) and may reflect the lack of adaptation to these evolutionarily novel stressors. The mechanisms of the exceptional mitochondrial resilience to temperature, salinity, and hypoxic stress are not yet fully understood in intertidal organisms, yet recent studies demonstrate that they may involve rapid modulation of the ETS capacity (possibly due to post-translation modification of mitochondrial proteins), upregulation of antioxidant defenses in anticipation of oxidative stress, and high activity of mitochondrial proteases involved in degradation of damaged mitochondrial proteins. With rapidly developing molecular tools for non-model organisms, future studies of mitochondrial adaptations should pinpoint the molecular sites associated with the passive tolerance and/or active regulation of mitochondrial activity during stress exposures in intertidal organisms, investigate the roles of mitochondria in transduction of stress signals, and explore the interplay between bioenergetics and mitochondrial signaling in facilitating survival in these highly stressful environments.