A Low Temperature Limit for Life on Earth

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.

The thermal limits to life on Earth

“…Currently identified upper thermal limits for growth are 122°C for archaeans, 100°C for bacteria and *60°C for unicellular eukaryotes. No unicells appear to grow below −20°C, a limit that is probably set by dehydration-linked vitrification of the cell interior driven by freeze-concentration in the presence of extracellular ice (Clarke et al 2013).…”

“…For example in the yeast Saccharomyces cerevisiae intracellular ice formation requires cooling rates faster than 20 K min − 1 (Seki et al 2009). Atmospheric cooling rates in the environment rarely exceed 1 K min − 1 (Clarke et al 2013), but some specialized habitats such as rock or leaf surfaces can change temperature more rapidly (Strimbeck et al 1993). Freezing of extracellular fluids does, however, occur in some multicellular plants and animals living in seasonally cold climates (Schmid 1982;Leather et al 1993;Pearce 2004).…”

“…In free-living unicells, dehydration driven by freeze-concentration of the external environment triggers vitrification at temperatures between −10 and −25°C (Clarke et al 2013).…”

Astrobiology and the Possibility of Life on Earth and Elsewhere…

“…Many of the limits are also caused by the detrimental influence of physical and chemical extremes on the capacity for cell metabolism, which may itself entail damage to macromolecules. For example, the lower limit for life may be defined by the temperature at which cytosol vitrification occurs, limiting cell activity (Clarke et al 2013). Ultimately the extremes of life are defined by the conditions under which the organisms can no longer harvest sufficient energy to repair or overcome the detrimental effects of stress and background mutation (Hoehler et al 2007).…”

Contrasting strategies of resistance vs. tolerance to desiccation in two polar dipterans

“…The responses of B. antarctica in this regard have been particularly well studied. Larvae accumulate glycerol and trehalose, which are suggested as being replacements for lost water and/or an aid to the production of amorphous sugar glasses (Danks 2000;Benoit, LopezMartinez et al 2007;Michaud et al 2008;Bahrndorff et al 2009;Benoit et al 2009;Hengherr et al 2009;Clarke et al 2013). Protein denaturation is also ameliorated via the up-regulation of HSPs in response to desiccation Teets et al 2012), and the fluidity of the membrane maintained using enzymes such as D9 FAD desaturase (LopezMartinez et al 2009).…”