Competitive inhibition of cobalt uptake by zinc and manganese in a pacificProchlorococcusstrain: 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.

Limitation by Fe, Zn, Co, and B12 Results in Similar Physiological Responses in Two Antarctic Phytoplankton Species

“…Other studies have described similar physiological responses of phytoplankton to limitation by Zn (Sunda and Huntsman, 1992;Sinoir et al, 2012Sinoir et al, , 2017, Co Hawco and Saito, 2018), and B 12 (Tang et al, 2010;Bertrand et al, 2012;Koch et al, 2013;Cohen et al, 2017). Some studies looked at the effects of limitation by one TM on the uptake/cellular quota of another (Sunda and Huntsman, 2004;Annett et al, 2008;Hawco and Saito, 2018). While these typically focused on the limitation of one or two TMS, they yielded important new concepts such as the biodilution of TMs (Sunda and Huntsman, 1998), the substitution of one TM for another (Sunda and Huntsman, 1995;Timmermans et al, 2001) and the classification of different limitation and co-limitation scenarios .…”

“…Typically Fe-limited cells grow more slowly, are often smaller, alter their photophysiology and have reduced particulate organic carbon (POC) quotas. Other studies have described similar physiological responses of phytoplankton to limitation by Zn (Sunda and Huntsman, 1992;Sinoir et al, 2012Sinoir et al, , 2017, Co Hawco and Saito, 2018), and B 12 (Tang et al, 2010;Bertrand et al, 2012;Koch et al, 2013;Cohen et al, 2017). Some studies looked at the effects of limitation by one TM on the uptake/cellular quota of another (Sunda and Huntsman, 2004;Annett et al, 2008;Hawco and Saito, 2018).…”

Nanoparticle Mediated NADPH Regeneration for Enhanced Ethanol Production by EngineeredSynechocystissp. PCC 6803

“…Another metal, Mn is also acting as a cofactor for superoxide dismutase and catalase, butit reduces the growth (Fig. 1a) by competitively inhibiting the intake of other cofactors at higher concentration (36). As a cofactor, Mo plays an important role in nitrogen assimilation with the combination of Fe-Mo, where the higher Mo concentration interferes with the Fe balance inside the cell and further reduces the growth of cyanobacteria (37).…”

Reannotation of the ribonucleotide reductase in a cyanophage reveals life history strategies within the virioplankton

“…Cytoplasmic cyanobacterial iron and 397 manganese quotas have been documented at 10 6 atoms/cell (Keren et al, 2002(Keren et al, , 2004) and a study that 398 aimed to identify and quantify metals in a cyanobacterium found that iron was present in high 399 intracellular concentrations, while cobalt concentrations were below the detection limit (Barnett et 400 al., 2012). Furthermore, some Prochlorococcus are able to maintain growth while up-taking just one 401 atom of cobalt per cell per hour (Hawco and Saito, 2018). Therefore, upon infection, a cyanophage 402 would encounter an intracellular pool of iron many fold larger than that of B12.…”