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

Abstract

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.

Fig. 1.

A schematic representation of marine primary productivity during the modern (A) and postulated Proterozoic (B). Geochemical cycles not directly related to primary productivity are neglected for simplicity. Dark heavy arrows reflect exit channels. Letters associated with fluxes are as follows: a, anoxygenic photosynthesis; b, oxygenic photosynthesis; c, sulfur oxidation by disproportionation or (non)phototrophic S-oxidizers; d, S⁰ respiration; e, sulfate reduction; f, S⁰-OM export/ballasting; g, pyrite formation; h, aerobic respiration; i, OM export; and j, O₂ export. (A) Primary productivity performed by oxygenic photosynthesis and where O₂ and CH₂O (OM) are produced in stoichiometric proportions. Light penetrates to a given depth, and due to available O₂, Eh remains high throughout the water column. Only within the sediments is O₂ exhausted and sulfide allowed to accumulate, both encapsulated by a decrease in Eh. (B) A mixed community of primary producers, with surface oxygenic photosynthesis dominated by cyanobacteria (rather than algae) and subchemocline anoxygenic photosynthesis driven by sulfide. Here, OM production reflects the sum of all primary production pathways, which is balanced by the production of O₂ in surface waters and S⁰ (or other oxidative intermediates: All represented as S_int) below the chemocline. As O₂ is depleted and sulfide concentrations increase, appreciable pools of S_int could accumulate. Light again decreases with depth, and as O₂ decreases across the chemocline, Eh would drop sharply. The specific chemistry of deep water will contribute to burial efficiencies, but is not central to our argument.

Fig. 2.

A schematic view of feedbacks that acted to sustain Proterozoic environments on both short and long geologic time scales (A and B, respectively). The point of entrance into this cycle is the establishment of sulfidic conditions at ≈1,840 Ma (5) and possibly earlier. Dashed green and solid red arrows note the direction of the feedback. If an increase in one quantity is followed by a decrease in the next, the connecting arrow is red (a negative feedback). If an increase in one quantity leads to an increase in the next, then the connecting arrow is green (a positive feedback). For example, if we begin in A with an increase in OMZ sulfide, P_O2 correspondingly decreases (thus a red arrow preceding the P_O2 ellipse), propagating responses through the remainder of the system. The presence of sulfide increases the likelihood of anoxygenic (by cyanobacteria, purple S bacteria, and/or green S bacteria) contributions to primary productivity, which would then produce less overall O₂, encourage N₂ fixation, increase primary production and carbon export, and increase the degree of euxinia (a positive feedback). (B) A sulfide-rich ocean in which S⁰ is an oxidant byproduct of primary producers and provides sedimentary conditions conducive to burial of both pyrite and carbon, although the burial of anoxygenically produced carbon is not strictly coupled to residual O₂ (no O₂ left behind). The loss of sulfide through pyrite burial dampens the extent of ocean euxinia (a negative feedback). The result is a system that maintains both oxygenic and anoxygenic photosynthesis.

Fig. 3.

A timeline showing OMZ chemistry (1–4, 7–10, 13, 14, 17), the relative contributions from different primary producers (17, 55, 69), and the evolution of eukaryotic heterotrophs (55–59, 70, 71). Band thicknesses approximate the importance of each feature through time. Dashed lines represent postulated or uncertain histories. The specific evolutionary sequence of oxygenic and anoxygenic photoautotrophs (including both cyanobacteria and purple/green S bacteria), marked here by **, rests in the Archean rock record (>2,500 Ma). As both processes had evolved by 1,800 Ma (23) (when our story begins), we make, nor require, any distinct sequence. The two thicker vertical lines represent the major Neoproterozoic glaciations (72), and the thinner line to the right marks the Ediacaran Gaskiers glaciation. The precise timing of Neoproterozoic climatic and biogeochemical events is the subject of ongoing research. We highlight the mixed contributions to primary productivity through the Proterozoic, a transition in OMZ chemistry at 800–700 Ma, and the coincident change in cyanobacteria, algal, protist, and animal abundances, based on body and molecular fossils.