Challenges during diapause and anhydrobiosis: Mitochondrial bioenergetics and desiccation tolerance

In preparation for the onset of environmental challenges like overwintering, food limitation, anoxia, or water stress, many invertebrates and certain killifish enter diapause. Diapause is a developmentally-programed dormancy characterized by suppression of development and metabolism. For embryos of Artemia franciscana (brine shrimp), the metabolic arrest is profound. These gastrula-stage embryos depress oxidative metabolism by ~99% during diapause and survive years of severe desiccation in a state termed anhydrobiosis. Trehalose is the sole fuel source for this developmental stage. Mitochondrial function during diapause is downregulated primarily by restricting substrate supply, as a result of inhibiting key enzymes of carbohydrate metabolism. Because proton conductance across the inner membrane is not decreased during diapause, the inference is that membrane potential must be compromised. In the absence of any intervention, the possibility exists that the F₁ F_o ATP synthase and the adenine nucleotide translocator may reverse, leading to wholesale hydrolysis of cellular ATP. Studies with anhydrobiotes like A. franciscana are revealing multiple traits useful for improving desiccation tolerance that include the expression and accumulation late embryogenesis abundant (LEA) proteins and trehalose. LEA proteins are intrinsically disordered in aqueous solution but gain secondary structure (predominantly α-helix) as water is removed. These protective agents stabilize biological structures including lipid bilayers and mitochondria during severe water stress. © 2018 IUBMB Life, 70(12):1251-1259, 2018.