Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age.

Molecular oxygen (O(2)) began to accumulate in the atmosphere and surface ocean ca. 2,400 million years ago (Ma), but the persistent oxygenation of water masses throughout the oceans developed much later, perhaps beginning as recently as 580-550 Ma. For much of the intervening interval, moderately oxic surface waters lay above an oxygen minimum zone (OMZ) that tended toward euxinia (anoxic and sulfidic). Here we illustrate how contributions to primary production by anoxygenic photoautotrophs (including physiologically versatile cyanobacteria) influenced biogeochemical cycling during Earth's middle age, helping to perpetuate our planet's intermediate redox state by tempering O(2) production. Specifically, the ability to generate organic matter (OM) using sulfide as an electron donor enabled a positive biogeochemical feedback that sustained euxinia in the OMZ. On a geologic time scale, pyrite precipitation and burial governed a second feedback that moderated sulfide availability and water column oxygenation. Thus, we argue that the proportional contribution of anoxygenic photosynthesis to overall primary production would have influenced oceanic redox and the Proterozoic O(2) budget. Later Neoproterozoic collapse of widespread euxinia and a concomitant return to ferruginous (anoxic and Fe(2+) rich) subsurface waters set in motion Earth's transition from its prokaryote-dominated middle age, removing a physiological barrier to eukaryotic diversification (sulfide) and establishing, for the first time in Earth's history, complete dominance of oxygenic photosynthesis in the oceans. This paved the way for the further oxygenation of the oceans and atmosphere and, ultimately, the evolution of complex multicellular organisms.

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 NH(4)(+) and NO(2)(-). 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 NO(3)(-) 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 NO(3)(-) 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.