Competitive inhibition of cobalt uptake by zinc and manganese in a pacific Prochlorococcus strain: Insights into metal homeostasis in a streamlined oligotrophic cyanobacterium

Abstract

In order to satisfy metabolic requirements for growth, marine cyanobacteria such as Prochlorococcus must acquire cobalt from seawater and synthesize cobalamin cofactors. Through a series of experiments with Prochlorococcus strain MIT 9215 under cobalt limiting conditions, the mechanism of Prochlorococcus' cobalt uptake was investigated. Due to low quotas, Prochlorococcus MIT 9215 can maintain growth at extremely slow rates of cobalt uptake, circa 1 atom per cell per hour. Cobalt quotas were linearly related to the concentration of inorganic cobalt species, Co′, indicating that the metal binding sites on the transporter are strongly unsaturated with respect to cobalt. When limited by cobalt, Prochlorococcus growth rates decreased at high levels of both Zn and Mn, suggesting that both metals compete with cobalt for the same transporter. This effect was not observed under a wide range of Fe, Cu, and Ni concentrations, although the onset of exponential growth was delayed at high Ni. These observations agree with prior characterizations of the periplasmic manganese binding protein MntC, which is probably the main pathway for inorganic cobalt uptake and the locus for Mn and Zn competitive inhibition. The toxicity of zinc toward cobalt limited Prochlorococcus MIT 9215 contrasts with the observation of cobalt-zinc substitution in eukaryotic phytoplankton and is expected to occur at environmentally relevant concentrations of free zinc and cobalt ions. Thus, the ecological success of Prochlorococcus in the modern ocean may depend on access to cobalt complexed by strong organic ligands that are not subject to competitive inhibition by other metals.