An abiotic source of Archean hydrogen peroxide and oxygen that pre-dates oxygenic photosynthesis

The evolution of oxygenic photosynthesis is a pivotal event in Earth’s history because the O2 released fundamentally changed the planet’s redox state and facilitated the emergence of multicellular life. An intriguing hypothesis proposes that hydrogen peroxide (H2O2) once acted as the electron donor prior to the evolution of oxygenic photosynthesis, but its abundance during the Archean would have been limited. Here, we report a previously unrecognized abiotic pathway for Archean H2O2 production that involves the abrasion of quartz surfaces and the subsequent generation of surface-bound radicals that can efficiently oxidize H2O to H2O2 and O2. We propose that in turbulent subaqueous environments, such as rivers, estuaries and deltas, this process could have provided a sufficient H2O2 source that led to the generation of biogenic O2, creating an evolutionary impetus for the origin of oxygenic photosynthesis.

basin in the Archean, respectively.
Without surface vegetation coverage on the land, an Archean river should carry suspended sediments like today's Yellow River, which has a mean solid concentration of 25 kg m -3 (ref. 1 ). In the suspended solids, quartz can account for up to 40 wt.% and its specific surface area is 0.1 m 2 g -1 (ref. 2 ), thereby the concentration of H2O2 in the river approaching the delta is 9.65 nM. Assuming the velocity of the river flow to the delta is 1 m s -1 (ref. 1 ), the amount of H2O2 passed through the cross section (100 cm 2 ) per second is 96.5 nmol (Supplementary Figure 9a), i.e., 0.965 nmol cm -2 s -1 . The H2O2 flux to the delta is calculated to be 5.81 × 10 14 molecules cm -2 s -1 .
The quartz on an Archean sandy beach would be under constant and intense friction by waves and tides. To estimate the in-situ flux of H2O2 of the coastal water at the Archean delta/shore, we use a small wedge-shaped unit of water column with a width of 1 cm and a depth of 0.2 m to calculate the H2O2 production in 1 year. If the angle of the slope near the sand beach is 7°, the volume of the wedge-shaped water column with a cross-section of 20 cm 2 is 1.63 L, which could carry about 407.5 g of quartz sand (Supplementary Figure 9b). The tumbling barrel experiments indicated that the increasing rate of the specific surface area of quartz in this specific hydrodynamic environment is 129.75 m 2 g -1 yr -1 (Supplementary Figure 8c). The total area of fresh surface produced in the water column in 1 year is 52863.52 m 2 . By multiplying to the H2O2 production on the unit surface area of quartz, the amount of H2O2 generated in the water column is calculated to be 5.11 × 10 -4 mol yr -1 . Thus, the in-situ flux of H2O2 diffusing across the section (20 cm 2 ) toward the open ocean is 4.87 × 10 11 molecules cm -2 s -1 .

The redox evolution of two locally oxidized environments in the Archean
The oxidants generated at the quartz-water interface would have led to the formation of oxygen oasis and driven the redox evolution in local aqueous environments in the Archean. To present a clear comparison with atmospheric photochemistry, we took the two calculated values of H2O2 flux into the quantitative model developed by McKay and Hartman (1991) 3 to simulate the redox evolution in Archean deltas and shores.
The dissolved ferrous iron was assumed to be the dominant reductant in Archean shallow seawater 4 , and the concentration was set to 100 μM. As Fe(II) will be oxidized to Fe(III) rapidly by the H2O2 or its decayed product (O2) when they diffuse across the oxic-anoxic interface, the reaction between Fe(II) and oxidants is not rate-limited but is determined by the diffusive transport of H2O2 through the oxic zone. Thus, we used the continuity equation (1) to describe the transport of H2O2 per unit area in the oxic zone, where L is the horizontal length of the oxic front that is the path of the mechanical/chemical H2O2 transport (the L is replaced by Z, the vertical depth of the oxic zone that is caused by the photochemically produced      Figure 7 The relationship between H2O2 production at the quartzwater interface and the particle size of quartz. For the fresh surface of 1 kg quartz with a grain size of 0.1 mm exposed in water, the H2O2 production is about 218 nmol.  5 which suggests that the resultant trace-level O2 is insufficient to fuel early respiration (dissolved O2 > 3 nM). c-d A steady transport of mechanical/chemical H2O2 into shallow seawaters in the Archean when the H2O2 flux is 5.81 × 10 14 molecules cm -2 s -1 (Fd, in a river approaching the delta, see Supplementary Text) and 4.87 × 10 11 molecules cm -2 s -1 (Fs, in seawater near shores, see Supplementary Text), respectively. After about 10 4 yr, the H2O2 concentration can be maintained at high levels (about 4 × 10 -4 M) in the oxic zone near the delta (L = 100 m), and about 4 × 10 -6 M for that near the shore (L = 10 m), respectively. Without considering the catalytic decomposition of H2O2 by peroxidases and catalases, the theorical H2O2 concentrations in both Archean locally oxidized environments are higher than the concentration of photochemically generated H2O2 in the upper layers of the present-day oceans (~10 -7 M) 6,7 . Our calculations suggest that compared with the atmospheric photochemistry, the mechanical abrasion by currents on quartz could effectively deplete initial reductants and provide oxidants (H2O2 and O2) for the phototrophs. These oxidants might have been enough to promote the development of oxygen tolerance and initiate the origin of oxygenic photosynthesis beneath an oxygen-poor atmosphere. (nM)