Abstract
There is no generally accepted value for the lower temperature limit for life on Earth. We present empirical evidence that free-living microbial cells cooling in the presence of external ice will undergo freeze-induced desiccation and a glass transition (vitrification) at a temperature between −10°C and −26°C. In contrast to intracellular freezing, vitrification does not result in death and cells may survive very low temperatures once vitrified. The high internal viscosity following vitrification means that diffusion of oxygen and metabolites is slowed to such an extent that cellular metabolism ceases. The temperature range for intracellular vitrification makes this a process of fundamental ecological significance for free-living microbes. It is only where extracellular ice is not present that cells can continue to metabolise below these temperatures, and water droplets in clouds provide an important example of such a habitat. In multicellular organisms the cells are isolated from ice in the environment, and the major factor dictating how they respond to low temperature is the physical state of the extracellular fluid. Where this fluid freezes, then the cells will dehydrate and vitrify in a manner analogous to free-living microbes. Where the extracellular fluid undercools then cells can continue to metabolise, albeit slowly, to temperatures below the vitrification temperature of free-living microbes. Evidence suggests that these cells do also eventually vitrify, but at lower temperatures that may be below −50°C. Since cells must return to a fluid state to resume metabolism and complete their life cycle, and ice is almost universally present in environments at sub-zero temperatures, we propose that the vitrification temperature represents a general lower thermal limit to life on Earth, though its precise value differs between unicellular (typically above −20°C) and multicellular organisms (typically below −20°C). Few multicellular organisms can, however, complete their life cycle at temperatures below ∼−2°C.
Highlights
Biologists have long been interested in the physical limits to life, in relation to life in extreme environments on Earth and the possibility of life elsewhere in the universe
Under the experimental conditions used, any intracellular freezing would have been detected by the release of latent heat associated with the change in entropy that accompanies the phase transition from liquid water to ice in the cell during cooling, or the reverse during warming; none was seen
Any glass transition events in the extracellular compartment would be expected to be at a lower temperature, but were not detected in this study because the volume of extracellular medium was so low in relation to that of the cells (Figure 2) as to render any Tg signal undetectable
Summary
Biologists have long been interested in the physical limits to life, in relation to life in extreme environments on Earth and the possibility of life elsewhere in the universe. The survival of bacteria and unicellular eukaryotes has been demonstrated down to 218uC in unfrozen hypersaline polar lakes [3,4,5], but in these extreme environments active cell division is typically confined to summer when shallow waters are warmed and illuminated by the sun. We present theoretical arguments and empirical evidence which clarify the biophysical constraints that determine the lower temperature limit for life on earth. Whilst photosynthesis has been reported in the Antarctic lichen Umbilicaria aprina at 217uC [6], spoilage of frozen food by the yeast Rhodotolura glutinis at 218uC [7] and metabolism of bacteria from permafrost at 220uC [8,9], the lower temperature limit for cell growth and division remains unclear [2].
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