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

Abstract

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.

Tectonically-driven oxidant production in the hot biosphere

“…The differences in the energy of crushing may have contributed to the differences in H 2 O 2 generation in the two room temperature studies. H 2 O 2 was detected in experiments when quartz was crushed for 5 h in a planetary ball mill at 350 rpm 5 , generating high mineral surface areas, but not after lower energy ‘end-over-end’ abrasion over a longer period of time 20 . In addition, high-energy planetary ball milling 5 may increase the temperature of mineral surfaces during the crushing process.…”

“…H 2 O 2 was detected in experiments when quartz was crushed for 5 h in a planetary ball mill at 350 rpm 5 , generating high mineral surface areas, but not after lower energy ‘end-over-end’ abrasion over a longer period of time 20 . In addition, high-energy planetary ball milling 5 may increase the temperature of mineral surfaces during the crushing process. After our planetary ball milling (30 min at 500 rpm) the bulk temperatures of the crushed rocks increased by 10.7 ± 0.6 °C (Methods).…”

“…A likely source of additional oxidants is peroxy bridges (Si–O–O–Si); ubiquitous oxidised defects within crystalline igneous and metamorphic rocks 5 , 6 , 10 , 22 . The average concentration of peroxy bridges within crystalline igneous and metamorphic rocks is 100 ppm 6 ; equivalent to 2940 nmol g −1 .…”

“…Two room temperature studies that have crushed both quartz and added water under a nitrogen atmosphere have generated either no detectable H 2 O 2 20 , or much lower H 2 O 2 concentrations (30 and 36 nmol g −1 at sediment loadings of 0.4 and 0.6 g mL −1 5 ), compared to 100 s to 1000 s nmol g −1 at 104 °C at a sediment loading of 0.5 g mL −1 in our experiments (Figs. 2 , 3 ).…”

“…It has been proposed that peroxy linkages could have been a source of H 2 O 2 to the subsurface prior to the evolution of photosynthesis 6 . It has been further suggested that mineral abrasion powered by streams, rivers and oceans would have generated SiO• and cleaved peroxy linkages on fractured silicate surfaces on the surface of the early Earth, perhaps generating sufficient H 2 O 2 for ancestors of modern-day cyanobacteria to use H 2 O 2 instead of H 2 O as a transitional electron donor to drive the evolution of oxygenic photosynthesis 5 .…”