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

• Arginase activation by Cu2+ is a unique characteristic of N. concinna.
• Muscular arginase can be linked to phosphagen breakdown.
• Arginases resistant to inhibition by heavy metals as an adaptive microevolution.
• Gills have the highest levels of arginase.

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±3.4 mmol L−1, may be involved in the control of l-arginine levels during phosphagen breakdown. N. concinna arginases showed the following preferences for metal cations: Ni2+>Mn2+>Co2+>Cu2+ in muscle and Mn2+>Cu2+ in gills. Cu2+ activation is a unique characteristic of N. concinna arginases, as copper is a potent arginase inhibitor. Cu2+ partly neutralized N. concinna arginase inhibition by Cd2+, worked synergistically in muscle arginase activation by Co2+ and neutralized muscle arginase activation by Ni2+. Mn2+ was able to activate muscle arginase in the presence of Fe3+ and Pb2+. The selection of arginases that are activated by Cu2+ and resistant to inhibition by Cd2+ in the presence of Cu2+ over evolutionary timescales may have favored N. concinna occupation of copper- and cadmium-rich niches.