Differential Responses of Prokaryotes and Eukaryotes to Fe-Stress: Possible Evolutionary Implications

Molecular and body fossils indicate that both eukaryotic algae and cyanobacteria existed in Proterozoic oceans. However, the record is dominated by cyanobacterial biomarkers suggesting their ecologically prominent role in marine primary production during this time. Why didn't eukaryotic algae begin to contribute significantly to marine primary production immediately after the Great Oxidation Event, 2.4 billion years ago (Ga)? Major shifts in transition metal availability tied to changes in ocean redox conditions could have been important because eukaryotes and prokaryotes respond differently to metal stress. To explore this concept, we investigated the biochemical responses of eukaryotic green algae and cyanobacteria to chronic Fe-deficiency. Iron deficiency would have arisen in ancient oceans as oxygen levels increased. We observed the intracellular Cu quota of the eukaryotic green alga, Chlamydomonas reinhardtii increase under chronic Fe-deficiency. This shift occurs because green algae replace key Fe proteins involved in photosynthetic electron transfer (e.g., cytochrome c6) with analogous Cu-based proteins (e.g., plastocyanin). In contrast, we found that the Cu quota of the cyanobacterium Synechocystis PCC6803 did not increase under chronic Fe-deficiency. Rather, intracellular Cu decreased. We hypothesize that, like eukaryotes, cyanobacteria respond to Fe-deficiency by producing compensatory proteins, but that these proteins either do not use Cu or reallocating intracellular Cu rather than increasing Cu content. The implication of these results is that cyanobacteria are better equipped than algae to cope with combined Fe- and Cu-deficiency. Such combined deficiencies may have been common in the oceans during much of the Proterozoic if a sulfide-rich, “Canfield ocean” prevailed, because of the low solubilities of Cu sulfides (as well as Fe sulfides). Eukaryotic algae would have encountered more favorable conditions when oxygen increased again in the Neoproterozoic, ushering in the Fe-poor but comparatively Cu-rich conditions typical of the Phanerozoic oceans.