Life in the slow lane: low rates of ubiquitin-dependent proteolysis in the heterothermic and heterometabolic tenrec, Tenrec ecaudatus.

Abstract

Classical mammalian hibernators, such as the golden-mantled ground squirrel, exploit cold temperatures typical of torpor (~ 4 °C) as a robust cue for an imprecisely-coordinated depression of homeostatic processes such as protein synthesis and degradation. As a result, torpid metabolic rates may be 1/100th of active rates in ground squirrels. Tenrecs have profound thermal and metabolic plasticity; active tenrecs housed at low ambient temperatures may have body temperatures and resting metabolic rates similar to torpid tenrecs or more similar to that of the basal metabolic rate of comparably sized mammals. Importantly, tenrecs may be more or less active or torpid at both high and low body temperatures. Thus, temperature is likely an inappropriate cue for the regulation of homeostatic processes. Here, we demonstrate tenrecs have low but highly variable (~ tenfold) ubiquitylated protein concentrations, maintain robust ubiquitylation rates in the cold, have depressed proteolytic activities in the cold, and do not experience a marked depression of proteolysis in the torpid state. These data suggest an inability to regulate protein degradation when torpid or when body temperatures are reduced. We suggest that in ancestral-like mammals, a suitable approach was 'Life in the Slow Lane', wherein rates of processes like protein degradation (and presumably protein synthesis) were simply slow regardless of body temperature or torpor status. Low rates of processes are congruent with observed low metabolic rates and would help mitigate homeostatic mismatches incurred by a lack of coordination that might otherwise be deleterious.