A reduction-dependent copper uptake pathway in an oceanic diatom

Abstract

Copper(II) is reduced to Cu(I) extracellularly by marine and freshwater phytoplankton, but its biological significance is not firmly established. We studied the relationship between Cu(II) reduction and uptake in Thalassiosira oceanica, a diatom that was recently shown to possess functional copper uptake transporters (CTRs) that take up Cu(I). Inorganic and organic complexes of Cu(II) were reduced directly by reactions at the cell surface in proportion to Cu(II)-ligand reduction potential. The rates of reduction were enhanced twofold in Cu-limited cells, suggesting reduction was regulated by Cu nutritional state. Suppressing Cu(II) reduction caused a decrease in Cu uptake rate by 97% and addition of a Cu(I) complexing agent completely inhibited cell division and reduced Cu quota when Cu concentration was growth limiting. Thus, Cu(II) reduction was an obligatory first step in Cu uptake. Cu(II) reduction rate and growth rate of T. oceanica were proportional to Cu–ethylenediaminetetraacetic acid concentration and independent of inorganic Cu concentration in bulk solution. The results suggest that Cu(II) bound to organic ligands was reduced by extracellular cupric reductases and subsequently internalized. This reduction-dependent uptake pathway may enable diatoms to use naturally occurring Cu(II) organic complexes in the sea.