Evidence of metabolic microevolution of the limpet Nacella concinna to naturally high heavy metal levels in Antarctica.

The gastropod Nacella concinna is the most conspicuous macroinvertebrate of the intertidal zone of the Antarctic Peninsula and adjacent islands. Naturally high levels of copper and cadmium in coastal marine ecosystems are accumulated in N. concinna tissues. We aimed to study the effects of metal cations on N. concinna arginase in the context of possible adaptive microevolution. Gills and muscle had the highest argininolytic activity, which was concentrated in the cytosol in both tissues. Gills had the highest levels of arginase and may be involved in the systemic control of l-arginine levels. The relatively high argininolytic activity of the N. concinna muscular foot, with KM=25.3±3.4mmolL(-1), may be involved in the control of l-arginine levels during phosphagen breakdown. N. concinna arginases showed the following preferences for metal cations: Ni(2+)>Mn(2+)>Co(2+)>Cu(2+) in muscle and Mn(2+)>Cu(2+) in gills. Cu(2+) activation is a unique characteristic of N. concinna arginases, as copper is a potent arginase inhibitor. Cu(2+) partly neutralized N. concinna arginase inhibition by Cd(2+), worked synergistically in muscle arginase activation by Co(2+) and neutralized muscle arginase activation by Ni(2+). Mn(2+) was able to activate muscle arginase in the presence of Fe(3+) and Pb(2+). The selection of arginases that are activated by Cu(2+) and resistant to inhibition by Cd(2+) in the presence of Cu(2+) over evolutionary timescales may have favored N. concinna occupation of copper- and cadmium-rich niches.