Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae

Marine primary producers adapted over eons to the changing chemistry of the oceans. Because a number of metalloenzymes are necessary for N assimilation, changes in the availability of transition metals posed a particular challenge to the supply of this critical nutrient that regulates marine biomass and productivity. Integrating recently developed geochemical, biochemical, and genetic evidence, we infer that the use of metals in N assimilation - particularly Fe and Mo - can be understood in terms of the history of metal availability through time. Anoxic, Fe-rich Archean oceans were conducive to the evolution of Fe-using enzymes that assimilate abiogenic NH4+ and NO2-. The N demands of an expanding biosphere were satisfied by the evolution of biological N-2 fixation, possibly utilizing only Fe. Trace O-2 in late Archean environments, and the eventual 'Great Oxidation Event' c. 2.3 Ga, mobilized metals such as Mo, enabling the evolution of Mo (or V)-based N-2 fixation and the Mo-dependent enzymes for NO3- assimilation and denitrification by prokaryotes. However, the subsequent onset of deep-sea euxinia, an increasingly-accepted idea, may have kept ocean Mo inventories low and depressed Fe, limiting the rate of N-2 fixation and the supply of fixed N. Eukaryotic ecosystems may have been particularly disadvantaged by N scarcity and the high Mo requirement of eukaryotic NO3- assimilation. Thorough ocean oxygenation in the Neoproterozoic led to Mo-rich oceans, possibly contributing to the proliferation of eukaryotes and thus the Cambrian explosion of metazoan life. These ideas can be tested by more intensive study of the metal requirements in N assimilation and the biological strategies for metal uptake, regulation, and storage.