Freeze tolerance: constraining forces, adaptive mechanisms

Abstract

For a variety of ectothermic animals, survival of subzero temperatures is aided by a natural capacity to tolerate extracellular freezing. Both low temperatures and freezing place inescapable constraints on the behaviour of molecules and biological structures. For example, low temperature affects metabolic rates, membrane fluidity, and weak bond interactions governing protein structure and function, whereas damage from freezing includes osmotic stress, membrane deformation, dehydration, physical damage by ice, and the consequences of long-term ischaemia. Selected biochemical adaptations permit survival of exposure to freezing by maintaining cell integrity, subcellular structure, energy production, and homeostasis. The key adaptations for freeze tolerance deal with the following: (i) control of extracellular ice: ice-nucleating proteins induce ice formation at multiple extracellular sites and at high subzero temperatures, whereas thermal hysteresis proteins inhibit the recrystallization of ice during long-term freezing; (ii) regulation of cell volume: the colligative action of high concentrations of polyols limit freeze concentration of the cell beyond a critical cell volume; (iii) protection of subcellular organization: trehalose and proline stabilize membrane bilayer structure, polyols stabilize protein structure; and (iv) viability in the frozen state: a well-developed tolerance for ischaemia plus mechanisms of facultative metabolic depression support long-term survival. Potential constraints of low temperature on metabolic functions are overcome to produce a metabolism that remains integrated and balanced over a wide temperature range. In addition, temperature change is exploited as a signal for the induction of various freeze tolerance adaptations.