The Glacier Ice Worm, Mesenchytraeus solifugus, Elevates Mitochondrial Inorganic Polyphosphate (PolyP) Levels in Response to Stress

SIMPLE SUMMARY: Energy maintenance in living organisms is crucial for survival. The ice-obligate worm, Mesenchytraeus solifugus, displays an unusual bioenergetic pattern, namely that intracellular ATP levels increase with declining temperature. In this study, we address the effects of stress on mitochondrial inorganic polyphosphate (polyP) and its relationship with ATP. Mitochondrial inorganic polyphosphate is a ubiquitous polymer whose role in the maintenance of prokaryotic and mammalian bioenergetics has been broadly demonstrated. We show here that polyP levels in ice worms increase with thermal stress, in contrast with those observed in other annelid worms. Thus, polyP may function as an energetic buffer in ice worms, effectively storing phosphate groups under stress and replenishing ATP under normal physiological conditions. ABSTRACT: The inorganic polymer, polyphosphate (polyP), is present in all organisms examined to date with putative functions ranging from the maintenance of bioenergetics to stress resilience and protein homeostasis. Bioenergetics in the glacier-obligate, segmented worm, Mesenchytraeus solifugus, is characterized by a paradoxical increase in intracellular ATP levels as temperatures decline. We show here that steady-state, mitochondrial polyP levels vary among species of Annelida, but were elevated only in M. solifugus in response to thermal stress. In contrast, polyP levels decreased with temperature in the mesophilic worm, Enchytraeus crypticus. These results identify fundamentally different bioenergetic strategies between closely related annelid worms, and suggest that I worm mitochondria maintain ATP and polyP in a dynamic equilibrium.