Acquisition of organically complexed copper by marine phytoplankton and bacteria in the northeast subarctic Pacific Ocean

Abstract

Copper (Cu) is an essential micronutrient for marine phytoplankton, but can cause toxicity at elevated intracellular concentrations. The majority of Cu (>99.9%) in oceanic surface waters is bound to strong organic ligands, presumably produced by prokaryotes to detoxify Cu. Although laboratory studies have demonstrated that organically complexed Cu may be bioavailable to marine eukaryotic phytoplankton, the bioavailability of Cu organic complexes to indigenous marine phytoplankton has not been examined in detail. Using the carrier free radioisotope 67Cu at an iron limited station in the northeast subarctic Pacific Ocean, we performed size fractionated short-term Cu uptake assays with three Cu(II)-chelates, and 67Cu bound to the strong in situ ligands, with or without additions of weak Cu(I) ligands. Estimates of the maximum supply of inorganic Cu (Cu′) to the cell surface of eukaryotic phytoplankton were unable to account for the observed Cu uptake rates from the in situ ligands and two of the three added Cu(II)-chelates. Addition of 10nM weak organic Cu(I) ligands enhanced uptake of Cu bound to the in situ ligands. Thus, Cu within the in situ and strong artificial Cu(II) organic ligands was accessible to the phytoplankton community via various possible Cu uptake strategies, including: cell surface enzymatically mediated reduction of Cu(II) to Cu(I), the substrate of the high-affinity Cu transport system in eukaryotes; or ligand exchange between weak Cu-binding ligands and the cellular Cu transporters. During a 14-hour uptake assay, particulate Cu concentrations reached a plateau in most treatments. Losses were observed in some treatments, especially in the small size fractions (<5μm), corresponding with faster initial Cu uptake rates. This may indicate that Cu cycling is rapid between particulate and dissolved phases due to cellular efflux or remineralization by micrograzers. The acquisition of Cu from the strong in situ ligands puts into question the historic role attributed to Cu binding ligands in decreasing Cu bioavailability.