Thermal Preference Ranges Correlate with Stable Signals of Universal Stress Markers in Lake Baikal Endemic and Holarctic Amphipods

Abstract

Temperature is the most pervasive abiotic environmental factor for aquatic organisms. Fluctuations in temperature range lead to changes in metabolic performance. Here, we aimed to identify whether surpassing the thermal preference zones is correlated with shifts in universal cellular stress markers of protein integrity, responses to oxidative stress and lactate content, as indicators of anaerobic metabolism. Exposure of the Lake Baikal endemic amphipod species Eulimnogammarus verrucosus (Gerstfeldt, 1858), Ommatogammarus flavus (Dybowski, 1874) and of the Holarctic amphipod Gammarus lacustris Sars 1863 (Amphipoda, Crustacea) to increasing temperatures resulted in elevated heat shock protein 70 (Hsp70) and lactate content, elevated antioxidant enzyme activities (i.e., catalase and peroxidase), and reduced lactate dehydrogenase and glutathione S-transferase activities. Thus, the zone of stability (absence of any significant changes) of the studied molecular and biochemical markers correlated with the behaviorally preferred temperatures. We conclude that the thermal behavioral responses of the studied amphipods are directly related to metabolic processes at the cellular level. Thus, the determined thermal ranges may possibly correspond to the thermal optima. This relationship between species-specific behavioral reactions and stress response metabolism may have significant ecological consequences that result in a thermal zone-specific distribution (i.e., depths, feed spectrum, etc.) of species. As a consequence, by separating species with different temperature preferences, interspecific competition is reduced, which, in turn, increases a species’ Darwinian fitness in its environment.

Nonspecific stress response to temperature increase in Gammarus lacustris Sars with respect to oxygen-limited thermal tolerance concept

“…Basal levels of both constitutive and stress-inducible HSP70 forms can vary significantly in different species and in separate populations of the same species when populations are adapted to different environmental conditions. Our previous study showed that in G. lacustris from a freshwater population (Irkutsk region), a significant nine-fold HSP70 elevation was observed under gradual temperature change up to 31 °C (Axenov-Gribanov et al, 2016). It is worth noting that multifold HSP70 accumulations in the freshwater population were observed immediately prior to the critical thermal mortality point of 100% individuals (Axenov-Gribanov et al, 2016).…”

“…Our previous study showed that in G. lacustris from a freshwater population (Irkutsk region), a significant nine-fold HSP70 elevation was observed under gradual temperature change up to 31 °C (Axenov-Gribanov et al, 2016). It is worth noting that multifold HSP70 accumulations in the freshwater population were observed immediately prior to the critical thermal mortality point of 100% individuals (Axenov-Gribanov et al, 2016). The results of the current study demonstrate that such multifold elevations of HSP70 levels do not occur in saltwater lake populations of G. lacustris .…”

“…It is known that in ambient temperature variation, the energy deficiency of cells increases due to a malfunction of the electron transport chain, which forces the organisms to activate less efficient energy recovery pathways, particularly in the anaerobic glycolysis pathway, leading to changes the activity of lactate dehydrogenase (Axenov-Gribanov et al, 2016). During glycolysis, lactate dehydrogenase catalyses in the reversible reaction of the pyruvate–lactate conversion.…”

“…In our previous studies we investigated inter-populational differences of energy metabolism during gradual warming in two distant populations of the common Holarctic amphipod Gammarus lacustris Sars, 1863 (Vereshchagina et al, 2016) from freshwater and saline lakes, and NCSR capacity of this species from the freshwater reservoir (Axenov-Gribanov et al, 2016). …”

“…In many organisms when exposed to stress conditions the amount of HSP70 is elevated due to the increase of damaged proteins (Axenov-Gribanov et al., 2016; Garbuz & Evgen’ev, 2017). Lactate dehydrogenase catalyzes the reaction of the interconversion of lactate and pyruvate and associated with the processes of carbohydrate and energy metabolism.…”