Eco-Evolutionary dynamics of oxygenic and anoxygenic photosyntheses in the late Archean.

The mechanisms that allowed the oxygenation of the Earth’s atmosphere to occur at the end of the Archean, an event known as the Great Oxidation Event (GOE), remain unclear. For the GOE to occur, two conditions must be met: first, oxygenic photosynthesis must evolve; second, the net production of dioxygen by photosynthesizers (i.e. the imbalance between carbon fixation and respiration corresponding to burial of organic matter), must exceed oxygen sinks such as reduced volcanic gases. Evidence points toward oxygenic photosynthesis evolving long before the traces of the GOE appear in the geological record. Thus, the oxygenation of Earth’s atmosphere may have been triggered by a combination of an increase in the burial flux of organic carbon (net O2 source) or a decreased O2 sink (e.g. via a decrease in the volcanic emissions of reduced gases). However, the drivers and dynamics of each of these processes are complex, and leveraging the geological record (e.g. stable carbon isotope record) to draw mechanistic conclusions about geochemical cycling at the time of the GOE remains challenging.

Recent modeling studies have highlighted the role of ecological competition for nutrient between anoxygenic and oxygenic photosyntheses as a potential driver for a delayed oxygenation of the atmosphere following the emergence of oxygenic photosynthesis (Ozaki et al 2019; Olejarz et al 2021). Here, I use adaptive dynamics theory (Metz et al., 1992) to rigorously and efficiently model the outcome of ecological competition in the upper layer of the Archean ocean as a function of boundary conditions set by the compositions of the deep ocean and of the atmosphere. Using a separation of timescales assumption, I then use the steady-state outcome of this ecological model as a boundary condition in a simplified geochemical model of phosphorous and iron cycling, and atmospheric oxygen.

The model shows how small perturbations in the delivery rate of iron or phosphorous to the deep ocean can trigger reversible or irreversible global oxygenation events. I examine a scenario where the upper ocean is initially phosphorous-limited and photoferrotrophs (anoxygenic photosynthesis where the electron donor is soluble iron) competitively exclude oxygenic photosynthesis. Then I assume that delivery rates of iron and phosphorus evolve or are perturbed such that the upper ocean transitions to conditions where photoferrotrophs would be iron-limited, giving oxygenic photosynthesis a fitness advantage (owing to its use of abundant water as an electron donor). In this scenario, an initially rare variant performing oxygenic photosynthesis may take come to dominate phototrophic primary production while the total remains constant, if local oxidation of soluble iron by dioxygen is fast enough (i.e. if the pH is high enough). The model demonstrates that coexistence between anoxygenic and oxygenic photosyntheses may not prevent oxygenation of the atmosphere, if the total productivity is high enough, and determines conditions where small perturbation in the geochemical system can trigger reversible or irreversible atmospheric oxygenations.