Copper export contributes to low copper levels and copper tolerance in Emiliania huxleyi

Abstract

Previous studies have documented that the coccolithophore Emiliania huxleyi maintains lower cellular copper concentrations and is more tolerant to high copper than are many other species of marine algae. We confirm that in comparison to the diatom Thalassiosira pseudonana, E. huxleyi maintains substantially lower Cu levels while maintaining near maximal growth rates. Using the stable isotope 65Cu as a tracer, we show that a constitutive or rapidly induced mechanism for Cu efflux is present in Cu‐replete E. huxleyi cells. This was revealed during uptake experiments in which the accumulation of the isotopically enriched spike, as measured by the isotope fractionation, exceeded the total accumulated copper. Evidence of efflux was not observed during Cu uptake in T. pseudonana cells. In contrast, copper‐limited E. huxleyi cells exhibited no observable efflux during uptake over the same time period, though net uptake rates were similar to replete cells, suggesting that efflux is modulated by cellular copper needs. This Cu‐efflux mechanism is effective over a wide range of Cu concentrations, as E. huxleyi is able to maintain much lower cellular Cu levels than T. pseudonana during 4 h uptake experiments. Direct measurement of export from copper‐loaded cells provided further evidence of a very effective efflux mechanism in E. huxleyi, while loss of copper from T. pseudonana was considerably less. Improvements to cell washes to remove surface‐bound Cu were implemented.