Minimum cobalt and iron requirements of Prochlorococcus: predicting micronutrient limitation thresholds for the ocean’s most abundant photoautotroph

Despite very low concentrations of cobalt in marine waters, cyanobacteria in the genus Prochlorococcus retain the genetic machinery for the synthesis and use of cobalt-bearing cofactors (cobalamins) in their genomes. We explored cobalt metabolism in a Prochlorococcus isolate from the Equatorial Pacific Ocean (strain MIT9215) through a series of growth experiments under iron and cobalt limiting conditions. Metal uptake rates, proteomic measurements of cobalamin-dependent enzymes, and theoretical calculations all indicate that Prochlorococcus MIT9215 can sustain growth with less than 50 cobalt atoms per cell, approximately 100-fold lower than minimum iron requirements for these cells. Quantitative descriptions of Prochlorococcus cobalt limitation are used to interpret new observations of the cobalt distribution in the South Pacific Ocean, where surface concentrations are among the lowest measured globally but Prochlorococcus biomass is high. Overlap between iron-limited and cobalt-depleted waters helps to explain how cobalt-dependent metabolism can persist in marine cyanobacteria, but suggests that increased Fe supply from dust in past (and perhaps future) oceans may have forced cobalt limitation in wild Prochlorococcus.