Soil salinity increases survival of freezing in the enchytraeidEnchytraeus albidus

Abstract

SUMMARYEnchytraeus albidus is a freeze-tolerant enchytraeid found in diverse habitats, ranging from supralittoral to terrestrial and spanning temperate to arctic regions. Its freeze tolerance is well known but the effect of salinity in this strategy is still poorly understood. We therefore studied the combined effect of salinity (0, 15, 35, 50‰ NaCl) and sub-zero temperatures (−5, −14, −20°C) on the freeze tolerance of E. albidus collected from two distinct geographical regions (Greenland and Germany). A full factorial design was used to study survival, and physiological and biochemical end points. The effect of salinity on the reproduction of German E. albidus was also assessed. Exposure for 48h to saline soils prior to cold exposure triggered an increase in osmolality and decrease in water content. Worms exposed to saline soils had an improved survival of freezing compared to worms frozen in non-saline soils, particularly at −20°C (survival more than doubled). Differential scanning calorimetry measurements showed that the fraction of water frozen at −5 and −14°C was lower in worms exposed to 35‰ NaCl than in control worms. The lowering of ice content by exposure to saline soils was probably the main explanation for the better freeze survival in saline-exposed worms. Glucose increased with decreasing temperature, but was lower in saline than in non-saline soils. Thus, glucose accumulation patterns did not explain differences in freeze survival. Overall, the physiological responses to freezing of E. albidus from Greenland and Germany were similar after exposure to saline soils. Soil salinity up to 30‰ improved reproduction by a factor of ca. 10.

Age-related environmental gradients influence invertebrate distribution in the Prince Charles Mountains, East Antarctica

“…These taxa are found more often in highly saline areas (figure 3), predominantly encountered at MM and ME (figure 2 a ); arachnids and tardigrades, on the other hand, tend to be more abundant in patches of nutrient-rich locations, predominantly at ME and LT (figures 2 a , 3 and 4). The observed habitat preferences for different invertebrate taxa are linked to substrate salinity, because salinity may affect soil biodiversity through constraining the amount of available food or by affecting physiological functions [10], such as freeze tolerance [64]. While most invertebrates are confined to low-saline substrates due to physiological constraints (here mostly LT), more halo-tolerant invertebrate taxa may be able to feed on halo-tolerant micro-eukaryotes in areas of high salinity [65].…”

Effect of repeated freeze-thaw cycles on geographically different populations of the freeze tolerant wormEnchytraeus albidus(Oligochaeta)

“…Further, previous studies (Fisker et al, 2014;Calderon et al, 2009) proposed that the mobilized glucose stores are also important as a fuel when the animals are frozen. An earlier study of freeze-tolerant oligochaetes (D. octaedra) found that the ability to survive winter frost correlates with the size of glycogen reserves , but for E. albidus the relationship between winter survival and accumulation of glucose is generally weak (Slotsbo et al, 2008;Silva et al, 2013;Fisker et al, 2014). Here, we investigated whether the energy used for metabolism during the different treatments is primarily correlated to catabolism of glucose/glycogen or lipids.…”

“…Previous studies on freezetolerant insects and vertebrates have also suggested that metabolism can remain (partially) aerobic during freezing (Voituron et al, 2002;Sinclair et al, 2004;Sinclair et al, 2013), while a study of the freeze-tolerant worm D. octaedra indicated that metabolism was a mixture of aerobic and (mostly) anaerobic metabolism (Calderon et al, 2009). In the case of E. albidus, the aerobic metabolism is likely to be dependent on the relatively low ice content found in this species at −5°C (Patrício Silva et al, 2013).…”

“…Oligochaetes, including E. albidus, are no exception to these generalized responses. Thus, freeze-tolerant oligochaetes are characterised by a large build-up of glycogen reserves prior to winter, a large accumulation of cryoprotectants following freezing and a (moderate) metabolic depression during the frozen period (Berman and Leirikh, 1985;Holmstrup et al, 1999;Rasmussen and Holmstrup, 2002;Overgaard et al, 2007;Slotsbo et al, 2008;Calderon et al, 2009;Overgaard et al, 2009;Silva et al, 2013;Fisker et al, 2014). The relationship between winter survival and accumulation of glycogen and glucose is, however, more complex than first assumed, as accumulated glucose can serve both as a cryoprotectant and as a fermentable fuel (Calderon et al, 2009;Fisker et al, 2014).…”

Membrane properties of Enchytraeus albidus originating from contrasting environments: a comparative analysis

“…it tolerates internal ice formation) and it has a broad geographical distribution. Populations originating from different environmental conditions (from temperate to arctic environments) are all freeze tolerant, but have markedly different cold tolerance when examined in common garden experiments (Fisker et al 2014a, b;Patrício Silva et al 2013;Slotsbo et al 2008). As other freeze-tolerant oligochaete species, E. albidus mobilize high concentrations of glucose during freezing, which acts as a cryoprotectant and as a fuel for metabolism during overwintering (Fisker et al 2014b;Slotsbo et al 2008).…”