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This study aimed to investigate species-specific thermal adaptations of two endemic amphipod species differing in their thermal tolerance and one widespread Holarctic species by comparing long-term responses to cold and warm temperatures beyond their respective preference temperatures. We hypothesize that the Holarctic G. lacustris is limited at the extreme low temperature (i.e. 1.5 °C) preventing this species from establishing a stable population in Lake Baikal, whereas the Baikal endemic amphipods possessing specific thermal adaptations to maintain a high energy metabolism in winter at low temperatures.To test this hypothesis, we measured metabolic markers in long-term acclimated animals exposed to four different temperatures (i.e., 1.5 °C, 6 °C, 12 °C and 15 °C) including the respective preference temperature of each species. More specifically , we studied key metabolic enzyme activities, such as citrate synthase and cytochrome c and oxidase, to estimate aerobic energy production and lactate dehydrogenase as an indicator of anaerobic glycolysis. To better understand the metabolic output of these enzymes we studied metabolite contents such as ATP, lactate, and glycogen. Finally, we investigated activities of three antioxidant enzymes to evaluate the level of cellular stress. Overall, we could demonstrate significant differences of several markers between all three species and their responsiveness to temperature. Common patterns and their implications for the performance of the species in their habitats are discussed in the following.Metabolic properties at optimal temperaturesLong-term acclimation to the preferred (= optimal) temperatures allows maintaining homeostasis and avoids any stress related to the non-optimal thermal conditions. At these optimal temperatures, the aerobic scopes of the species should be at their maxima meaning that maximum excess oxygen is available to fuel processes above maintenance to support e.g., growth and reproduction7,27.Here, we found differences in the capacities of aerobic metabolism, levels of energy equivalents and energy stores between the three species, as indicated by the higher activity of cytochrome c oxidase, ATP and glycogen levels in G. lacustris compared to the two Baikal species. This is in line with our previous findings about routine metabolic rates, measured as oxygen consumption in the studied species21.Constantly low temperatures led to decreased cellular ATP levels and activities of cytochrome c oxidase in Baikal endemics, thereby indicating a reduced rate of basal metabolism. The same trend was observed in Antarctic fish compared to temperate and tropical fish species27,28.However, the activity of another marker of aerobic metabolism—citrate synthase—is similar among the three species. The higher citrate synthase/cytochrome c oxidase ratio in Baikal species compared to G. lacustris may be attributed to the prevalence of lipid over glucose metabolism in Baikal species29. Significantly higher levels of glycogen in G. lacustris support this assumption.Here, we studied one thermally tolerant Baikal endemic species, E. cyaneus, and one cold-stenothermal species, E. verrucosus. Previous studies on the molecular evolution of thermal tolerance revealed significant structural and functional differences in heat shock proteins (Hsp70), a universal molecular protection system24. Significant differences in routine metabolic rate and lethal temperatures were also shown21, supporting both endemic species’ thermal classification. The present results widen our mechanistic understanding of thermotolerance in Baikal amphipods. Particularly, when acclimated to their preferred temperatures, the two Baikal species showed some differences in metabolic fuel usage. Higher glucose, glycogen and lactate levels correspond to a more enhanced glucose metabolism, which may be required to maintain higher metabolic activity of the thermotolerant species E. cyaneus. However, capacities of cytochrome c oxidase and citrate synthase activities are similar, as well as the ATP level, which indicates similar rates of oxygen metabolism under optimal thermal condition in these two species.Oxygen metabolism is tightly connected with the antioxidative defense against reactive oxygen species (ROS) as they are natural byproducts of aerobic metabolism. Therefore, we studied the activity of three antioxidative enzymes. Our results indicate that despite higher aerobic capacities and presumably higher metabolic rates in G. lacustris compared to the two Baikal species, the activities of catalase and glutathione S-transferase were comparable and for peroxidase even higher in the cold stenothermal E. verrucosus than in G. lacustris (Fig. 2). Similarly, Abele and Puntarulo24,30 showed that the basic levels of superoxide dismutase activity in polar mollusks are higher than in temperate ones. Increased ROS generation in cells of ectothermic animals may occur due to higher oxygen solubility in cold water and biological fluids31,32. Thus, higher peroxidase level in E. verrucosus is likely an adaptation to the low temperatures with its high dissolved oxygen content in Baikal water.Glutathione S-transferase activities were found to be higher in both thermotolerant species—G. lacustris and E. cyaneus. Besides protecting against ROS, this enzyme has multiple functions, including xenobiotic detoxification33. Thus, its higher activity may be related to the enhanced tolerance level to various environmental factors in both species besides temperature.Thermal exposure to lower than the preferred temperaturesWe hypothesized that Baikal species have metabolic adaptations to cold temperatures that allow an active lifestyle in the cold. Thus, we expected cold compensation mechanisms (i.e., increased enzyme activities due to higher densities of mitochondria in cold stenotherms). Our results indicate that this is the case only for E. cyaneus (Baikal endemic, thermotolerant), as it showed increased cytochrome c oxidase activities at 1.5 °C. As the citrate synthase activity and ATP level remained unchanged, compensation of the respiratory chain seems to be sufficient to support stable energy production at low temperatures and an alteration of the mitochondrial ultrastructure, i.e., increased cristae density (cytochrome c oxidase) relative to the matrix (citrate synthase) may be involved in cold acclimation.E. cyaneus represents the rather small summer-reproducing complex among Baikal endemic amphipods. Despite its relatively high thermotolerance24, this species is actively moving under the ice cover in winter. In our experiments, animals of this species expressed high locomotor and feeding activity at all exposure temperatures, including 1.5 °C. Our results unravel the metabolic adaptation providing this rather wide thermotolerance window of this species. Already at 6 °C, glycogen started to accumulate, which also reoccurred at 1.5 °C. Glycogen accumulation is a well-known strategy of overwintering ectotherms known as cold hardiness, especially in those surviving in frozen habitats under oxygen-limited conditions34. Similar, we found an accumulation of glycogen above the control level in the Holarctic G. lacustris when exposed to 12 and 6 °C. However, at 1.5 °C the level of glycogen in this species was below the control level, indicating reduced glycogenesis possibly due to metabolic depression in the cold.Instead, E. cyaneus can maintain a high level of glycogenesis at 1.5 °C, and therefore accumulate glycogen in winter, despite its lower metabolic rate compared to G. lacustris. Surprisingly, at 6 °C we found a strong increase in lactate dehydrogenase activity in E. cyaneus, which was not followed by a significant accumulation of lactate or significant depletion of ATP indicating the absence of functional anaerobiosis. This unpredicted reaction of lactate dehydrogenase in this species at 6 °C, which is the Baikal littoral zone’s annual average temperature, requires further studies.Exposure to 1.5 °C and 6 °C caused decreased catalase and peroxidase activities and decreased lactate levels in E. cyaneus, which would be in line with a reduced metabolic rate, following the Q10 rule. Thus, our results indicate that E. cyaneus can maintain a high level of aerobic metabolism within a wide thermal range including the common winter temperature—1.5 °C. Although E. cyaneus is one of the most thermotolerant Baikal amphipod species, differences to the closely-related thermotolerant Holarctic G. lacustris became apparent as the latter failed to maintain high ATP and lactate levels at the lowest exposure temperature likely due to lacking compensation (citrate synthase, cytochrome c oxidase) or even inactivation of enzyme functions (including lactate dehydrogenase). This reduced energy state may likely contribute to the low locomotor activity of G. lacustris at the lowest exposure temperature.Surprisingly, no cold compensation in any of the studied parameters was found for the cold-loving Baikal endemic species E. verrucosus. This species belongs to the winter-reproducing complex, which is most common in the littoral zone. The absence in cold compensation of this species indicates that at 1.5 °C its energy metabolism remains on its physiological maximum.The absence of glycogen accumulation at low temperatures in this species can be explained by the food availability during winter in Lake Baikal’s littoral zone. Presumably, the existing amount of winter nutrition is sufficient for E. verrucosus to maintain maximum aerobic capacities and energy metabolism. The high nutrition allows the species to breed, develop eggs and release juveniles, which occurs during the seasons with lowest annual temperatures. Another explanation can be the usage of lipids instead of carbohydrates as energy source in winter. The lower amount of glycogen and free glucose than in the thermotolerant congener E. cyaneus, supports this hypothesis.Thus, despite the relatively similar aerobic capacities of the thermotolerant E. cyaneus and the winter-reproducing cold stenothermal E. verrucosus at their respective preference temperatures, the latter species shows a different metabolic fuel use, that allows E. verrucosus to maintain its maximum metabolic rate at 1.5 °C.We hypothesized that the Holarctic G. lacustris has disadvantages compared to the two Baikal species regarding energy metabolism at low temperatures. Gammarus lacustris is eurythermal and often overwinters in small ponds, which are nearly completely frozen in winter35. However, it has been shown that temperatures below its optimal range cause decreased respiration rates and activity possibly resulting in torpor21,35. Our observations confirmed these assumptions as at 1.5 °C individuals of G. lacustris significantly decreased their locomotor and feeding activities. The assumption that G. lacustris shows metabolic depression at 6 °C and 1.5 °C is supported by the decreased ATP, lactate, and lactate dehydrogenase activity levels. Moreover, only for this species we observed mortality at 1.5 °C, which indicates that this experimental thermal condition is stressful. This is supported by the increase in catalase activity over the control level and the elevated level of peroxidase activity at 1.5 °C, while at 12 °C and 6 °C, the capacity for this enzyme was decreased compared to the control (following the Q10 rule). In this case, exposure to 1.5 °C could cause cellular damages resulting in the development of oxidative stress. Preparation for such extreme temperatures for G. lacustris like requires enough time to accumulate cryoprotectors25 and adjust the metabolism in its natural habitat. Besides, we observed the accumulation of glycogen, like in the thermotolerant E. cyaneus. For G. lacustris, accumulation of glycogen for the wintertime is essential, as it is often overwintering in nearly completely frozen ponds and therefore experiences periods of hypoxia23. Glycogen can be metabolized via anaerobic glycolysis, in contrast to lipid storages, which require oxygen for their metabolizations34. In comparison to E. cyaneus, accumulation of glycogen over the control level in G. lacustris occurs already at 12 °C, indicating the lower thermal threshold of the zone of preferred temperatures for this species22, but this accumulation disappeared at the lowest temperature indicating that G. lacustris follows a different strategy for winter survival than cold hardiness34.Thermal exposure to higher than the preferred temperaturesPrevious studies indicated that 15 °C is the critical thermal threshold for large adults of the stenothermal E. verrucosus, and it was observed that most of these individuals start to migrate to deeper littoral zones when the temperature in the Baikal littoral surpass about 11 °C21. Thus, E. verrucosus is behaviorally adapted to escape deleterious temperatures. When exposed to gradual temperature increase, individuals of E. verrucosus showed accumulation of lactate and heat shock proteins at temperatures exceeding 12 °C22,24. Our results complement these previous findings, as lactate levels were significantly higher than the control lactate levels at 12 °C. At 15 °C, increases of lactate dehydrogenase capacities were detected, which may foster a higher turnover and remobilization of lactate at this temperature compared to 12 °C, as lactate level did not further increase. As shown earlier lactate dehydrogenase was the only metabolic enzyme exhibited similar kinetic and regulatory properties as the other two amphipod species (following simple Q10 rules)23. The results here confirm the need of E. verrucosus to keep higher anaerobic capacities and turnover rates at the upper limit of the thermal window, where functional hypoxia may appear7,27.In the more thermotolerant E. cyaneus, exposure to 15 °C caused increases of ATP, lactate, and both peroxidase and catalase activities. Increases of both ATP and lactate likely indicate the enhancement of the cellular respiration rather than the onset of anaerobiosis. Activation of peroxidase and catalase may indicate both the development of cellular stress and the general increase in metabolic rate following the Q10 rule. The last explanation is more likely, as antioxidant enzyme activities, lactate and ATP content gradually increased with rising temperature. As E. cyaneus is a sedentary species, that occupies a rather narrow zone of the upper littoral, such a metabolic plasticity can serve as a specific adaptation to its thermal niche. Opposite, for the migrating E. verrucosus, behavioral responses are more important when temperatures gradually increase. More

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AffiliationsEnergy and Resources Group, UC Berkeley and Climate and Ecosystem Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USALara M. KueppersAuthorsLara M. KueppersCorresponding authorCorrespondence to
Lara M. Kueppers. More