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Freeze Tolerance, Supercooling Points and Ice Formation: Comparative Studies on the Subzero Temperature Survival of Limno-Terrestrial Tardigrades

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Freeze Tolerance, Supercooling Points and Ice Formation: Comparative Studies on the Subzero Temperature Survival of Limno-Terrestrial Tardigrades 802 The Journal of Experimental Biology 212, 802-807 Published by The Company of Biologists 2009 doi:10.1242/jeb.025973 Freeze tolerance, supercooling points and ice formation: comparative studies on the subzero temperature survival of limno-terrestrial tardigrades S. Hengherr1, M. R. Worland2, A. Reuner1, F. Brümmer1 and R. O. Schill1,* 1Universität Stuttgart, Biological Institute, Department of Zoology, Pfaffenwaldring 57, 70569 Stuttgart, Germany and 2British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK *Author for correspondence (e-mail: [email protected]) Accepted 6 January 2009 SUMMARY Many limno-terrestrial tardigrades live in unstable habitats where they experience extreme environmental conditions such as drought, heat and subzero temperatures. Although their stress tolerance is often related only to the anhydrobiotic state, tardigrades can also be exposed to great daily temperature fluctuations without dehydration. Survival of subzero temperatures in an active state requires either the ability to tolerate the freezing of body water or mechanisms to decrease the freezing point. Considering freeze tolerance in tardigrades as a general feature, we studied the survival rate of nine tardigrade species originating from polar, temperate and tropical regions by cooling them at rates of 9, 7, 5, 3 and 1°C h–1 down to –30°C then returning them to room temperature at 10°C h–1. The resulting moderate survival after fast and slow cooling rates and low survival after intermediate cooling rates may indicate the influence of a physical effect during fast cooling and the possibility that they are able to synthesize cryoprotectants during slow cooling. Differential scanning calorimetry of starved, fed and cold acclimatized individuals showed no intraspecific significant differences in supercooling points and ice formation. Although this might suggest that metabolic and biochemical preparation are non-essential prior to subzero temperature exposure, the increased survival rate with slower cooling rates gives evidence that tardigrades still use some kind of mechanism to protect their cellular structure from freezing injury without influencing the freezing temperature. These results expand our current understanding of freeze tolerance in tardigrades and will lead to a better understanding of their ability to survive subzero temperature conditions. Key words: tardigrada, differential scanning calorimetry, DSC, supercooling point, SCP, cooling rate, cold tolerance INTRODUCTION against phase transition and to control the ice fraction size and Tardigrades can be found in a diversity of habitats including marine, minimum cell volume resulting from freeze concentration and freshwater and terrestrial ecosystems ranging from the deep sea to osmotic dehydration (Ramløv, 2000; Sinclair et al., 2003; the highest mountains (Nelson, 2002). Many limno-terrestrial Zachariassen, 1985). Ice active proteins are also sometimes present tardigrade species are able to tolerate harsh environmental conditions and may act as recrystallization inhibitors, which prevent the in any developmental stage (Schill and Fritz, 2008) by entering a growth and redistribution of ice crystals once these have formed cryptobiotic state which is induced by desiccation (anhydrobiosis), (Duman, 2001; Wharton, 2003). lack of oxygen (anoxybiosis), osmotic pressure (osmobiosis) or low A third survival strategy termed cryoprotective dehydration has temperatures (cryobiosis) (Keilin, 1959). In this state metabolism been observed in recent studies on the arctic springtail Onychiurus is undetectable and life comes to a reversible standstill until activity arcticus (Worland and Block, 2003; Worland et al., 1998) and the is resumed under favourable conditions (Keilin, 1959). In the Antarctic midge Belgica antarctica (Elnitsky et al., 2008). In this anhydrobiotic state, tardigrades and other cryptobiotes such as case, desiccation occurs due to the difference in water vapour nematodes and rotifers show extraordinary tolerance of physical pressure between the animal’s supercooled body fluids and ice in extremes including high and subzero temperatures, ionizing its surroundings (Elnitsky et al., 2008; Holmstrup et al., 2002; radiation, alcohols and high pressure (Horikawa et al., 2006; Worland and Block, 2003; Worland et al., 1998). Jönsson et al., 2008; Jönsson and Schill, 2007; Ramløv and Westh, Some organisms including the Antarctic nematode 2001; Rebecchi et al., 2007; Seki and Toyoshima, 1998). Panagrolaimus davidi even survive intracellular freezing (Smith et To survive exposure to temperatures below the freezing point of al., 2008; Wharton and Ferns, 1995; Wharton et al., 2003). Freeze their body fluids, cold tolerant organisms mainly use either the freeze tolerance in the tardigrade Richtersius (Adorybiotus) coronifer, avoidance or freeze tolerance strategy (Storey and Storey, 1996). originating from polar regions, has been reported previously by While freeze avoiding organisms depress the temperature of Westh and colleagues (Westh and Kristensen, 1992), with survival spontaneous freezing (supercooling point, SCP) by using antifreeze of freezing of more than 80% of the body water during exposure proteins and other cryoprotectants (e.g. sugars and polyols) (Danks to subzero temperatures. However, whether tardigrades also tolerate et al., 1994; Duman, 2001), ice formation of the extracellular body intracellular freezing or keep the cytoplasm in a liquid state either water is tolerated by freeze tolerant organisms and is often triggered by synthesizing cryoprotectants or by cryoprotective dehydration is at high temperatures by ice nucleating proteins (Lee and Costanzo, unknown. 1998; Ramløv, 2000). In many freeze tolerant organisms, polyols Tardigrades are well known to survive freezing in the and sugars are accumulated to protect membranes and proteins dehydrated state (Wright, 2001) but are also reported to survive THE JOURNAL OF EXPERIMENTAL BIOLOGY Freeze tolerance in tardigrades 803 exposure to –196°C fully hydrated (Ramløv and Westh, 1992; criticized as too fast compared with natural cooling rates (Sinclair Sømme and Meier, 1995). However, there have been very few et al., 2003). Natural cooling rates around 3 and 6°Ch–1 have been experimental studies concerning the ability of tardigrades to recorded in ecological studies on e.g. Drosophila melanogaster survive natural freezing conditions in a hydrated state (Ramløv (Kelty and Lee, 1999). To study the cold tolerance of tardigrades and Westh, 1992; Sømme and Meier, 1995; Westh and Hvidt, under ecologically relevant cooling rates, we used cooling rates 1990; Westh et al., 1991). In fact, few detailed studies have been of 9, 7, 5, 3 and 1°Ch–1. The tardigrades were exposed to the undertaken on cold tolerance as a general feature in any limno- cooling rates starting at room temperature (RT, 20°C) down to terrestrial organism. –30°C, followed by a warming period at 10°Ch–1 up to RT. Alive This study presents new data on the effect of various cooling and dead animals were recorded after thawing. Tardigrades were rates on the survival of nine different tardigrade species originating assumed to be dead if there was no movement visible within 2h from polar, temperate and tropical areas. SCPs of individual of rehydration. Four replicates per species were used for each tardigrades were obtained for the first time using differential cooling treatment (see Table1). scanning calorimetry (DSC) and the effects of gut content and acclimation to low temperatures on the SCP were investigated. While Calorimetry SCP measurements in previous studies were obtained using groups A Mettler-Toledo differential scanning calorimeter (DSC820, of tardigrades, which might be influenced by the nucleation activity Mettler-Toledo, Leicester, UK) was used to measure the SCP of the surrounding water resulting in one single freezing event for (=temperature of crystallization, Tc) and quantity of water freezing the whole group, this study provides the first data on SCPs of in tardigrades as they were cooled at 10°Cmin–1 from 25°C to 5°C individual tardigrades. and at 1°Cmin–1 from 5°C to –30°C. To obtain crystallization points for each individual the animals were placed in separate single MATERIALS AND METHODS droplets of water in aluminium pans. Residual water around each Tardigrades individual was removed with filter paper directly before the pans Laboratory reared and field collected tardigrades were used in this were hermetically sealed and placed in the calorimeter. After the study. Animals of the Eutardigrada species Macrobiotus sapiens determinations, the animals were checked visually for any indication Binda and Pilato 1984 were collected in Rovinj, Croatia. Specimens of dehydration resulting from a poorly sealed pan, which would of Milnesium tardigradum Doyère 1840 and Paramacrobiotus have a large effect on the SCP; data for such samples were not richtersi Murray 1911 were collected in Tübingen, Germany. The included in this study. The calorimeter was calibrated using indium species Macrobiotus tonollii Ramazzotti 1956 was from Eugene, as an upper temperature and enthalpy standard (melting point OR, USA (all temperate habitats). Paramacrobiotus richtersi ‘group 156.6°C, enthalpy 28.71Jg–1) and the melting point of ice as a lower 1’ was from Nakuru and Paramacrobiotus richtersi ‘group 2’ was temperature check. A standard temperature program starting at 25°C from Naivasha, Kenya (tropical
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