How do Antarctic notothenioid fishes cope with internal ice? A novel function for antifreeze glycoproteins

Abstract

Antarctic fishes survive freezing through the secretion of antifreeze glycoproteins (AFGPs), which bind to ice crystals to inhibit their growth. This mode of action implies that ice crystals must be present internally for AFGPs to function. The entry and internal accumulation of ice is likely to be lethal, however, so how do fishes survive in its presence? We propose a novel function for the interaction between internal ice and AFGPs, namely the promotion of ice uptake by splenic phagocytes. We show here that i) external mucus of Antarctic notothenioids contains AFGPs and thus has a potential protective role against ice entry, ii) AFGPs are distributed widely through the extracellular space ensuring that they are likely to come into immediate contact with ice that penetrates their protective barriers, and iii) using AFGP-coated nanoparticles as a proxy for AFGP adsorbed onto ice, we suggest that internal ice crystals are removed from the circulation through phagocytosis, primarily in the spleen. We argue that intracellular sequestration in the spleen minimizes the risks associated with circulating ice and enables the fish to store the ice until it can be dealt with at a later date, possibly by melting during a seasonal warming event.