A mineral-based origin of Earth's initial hydrogen peroxide and molecular oxygen - PubMed (original) (raw)

. 2023 Mar 28;120(13):e2221984120.

doi: 10.1073/pnas.2221984120. Epub 2023 Mar 20.

Hongping He 1 2 3, Jianxi Zhu 1 2 3, Mang Lin 2 3 4, Ying Lv 1 2 5, Haiyang Xian 1 2, Yiping Yang 1 2, Xiaoju Lin 1 2, Shan Li 1 2 3, Yiliang Li 6, H Henry Teng 7, Mark H Thiemens 8

Affiliations

A mineral-based origin of Earth's initial hydrogen peroxide and molecular oxygen

Hongping He et al. Proc Natl Acad Sci U S A. 2023.

Abstract

Terrestrial reactive oxygen species (ROS) may have played a central role in the formation of oxic environments and evolution of early life. The abiotic origin of ROS on the Archean Earth has been heavily studied, and ROS are conventionally thought to have originated from H2O/CO2 dissociation. Here, we report experiments that lead to a mineral-based source of oxygen, rather than water alone. The mechanism involves ROS generation at abraded mineral-water interfaces in various geodynamic processes (e.g., water currents and earthquakes) which are active where free electrons are created via open-shell electrons and point defects, high pressure, water/ice interactions, and combinations of these processes. The experiments reported here show that quartz or silicate minerals may produce reactive oxygen-containing sites (≡SiO•, ≡SiOO•) that initially emerge in cleaving Si-O bonds in silicates and generate ROS during contact with water. Experimental isotope-labeling experiments show that the hydroxylation of the peroxy radical (≡SiOO•) is the predominant pathway for H2O2 generation. This heterogeneous ROS production chemistry allows the transfer of oxygen atoms between water and rocks and alters their isotopic compositions. This process may be pervasive in the natural environment, and mineral-based production of H2O2 and accompanying O2 could occur on Earth and potentially on other terrestrial planets, providing initial oxidants and free oxygen, and be a component in the evolution of life and planetary habitability.

Keywords: H2O2 production; life evolution; oxygen transfer; quartz; surface radicals.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.

Fig. 1.

Two proposed mechanisms for H2O2 generation at quartz–water interfaces. (A) Stress-induced cleavage of Si–O bonds. Applied force is represented by a linear falling potential (dashed line), which is added to the Morse potential of the unstretched Si–O bond (dotted line), thus resulting in a force-deformed Morse potential (solid line). The new dissociation energy D′ is smaller than D in the case of a stretching force. Modified after Kauzmann et al. (42). The probability of generation of surface-bound radicals in quartz therefore increases during mechanical processes. (B) Contact of water on freshly fractured surface of abraded quartz. Modified after Schoonen et al. (32). (C) Generation of H2O2 and O2 in the reaction between H2O and oxygen radical (≡SiO•). (D) Generation of rocky H2O2 and O2 in the reaction between H2O and peroxy radical (≡SiOO•). Surface-bound radicals are formed through homolysis of Si–O bonds, including ≡SiO•, ≡SiOO•, and E′ center (≡Si•), while surface charges (≡Si+ and ≡SiO–) for heterolysis. Silanol groups (≡SiOH) are end products on quartz surface after hydroxylation.

Fig. 2.

Fig. 2.

XPS evidence for the formation of reactive sites on abraded quartz surface. (A and B) O 1_s_ and Si 2_p_ spectra of abraded quartz and intact quartz. The fitted peaks for the spectra of abraded quartz correspond to bridging oxygen (BO, i.e., ≡Si–O–Si≡ and ≡Si–O–O–Si≡) and nonbridging oxygen (NBO, i.e., ≡SiO–, ≡SiO•, ≡SiOO•). (C) Comparison between the valence band and O 2_s_ spectra of abraded quartz and intact quartz. The valence band spectrum is assigned to NBO orbitals (1_e_, 5_t_2, 1_t_1 orbitals) of mostly O 2_py_ character and BO σ-bonding orbitals (5_α1_, 4_t2_) of mostly Si sp_3–O 2_pz character. The O 2_s_ band consists of a main peak (3_t_2) and a shoulder (4_a_1). (D) A differential spectrum obtained by subtracting the spectrum of intact quartz from that of abraded quartz.

Fig. 3.

Fig. 3.

The generation and content of 18O labeled _p_-HBA in the 18O labeling experiments. (A) The scheme of the 18O-labeling experiments [Set I: QGN+BA(H218O); Set II: QGN+H218O; Set III: QGO+BA(H218O); Set IV: QGO+H218O]. (C) ROS production in the suspension of QGN. (B and D) The content of _p-_HBA(16OH) and _p-_HBA(18OH) that produced after QGN/QGO was added into BA(H218O) solution or H218O (Set I–IV experiments), respectively. The OTotal is the total O atoms from •OH and H2O2. The error bars present ±1 SD of three independent replicates.

Scheme 1.

Scheme 1.

The proposed oxygen transfer pathways in the hydroxylation of the peroxy radical (≡SiOO•). The H atom of water binds with the terminal oxygen of surface peroxy radical (≡SiOO•), while the O atom of water attaches to the Si atom of ≡SiOO•, so that peroxy oxygen pair (O–O) remains intact and the HO2• (perhydroxyl radical) is formed. Red letters indicate the rocky oxygen from silicates.

Fig. 4.

Fig. 4.

The rocky oxygen-driving evolution of ROS-detoxifying system in early life in the Archean. (A) ROS production in geological processes (e.g., earthquakes and river erosion). (B) Oxygen transfers during the ROS generation and conversion at interface between H218O and abraded quartz and ingestion by microorganisms. Early microorganisms coped with ROS by antioxidant enzymes. For example, the H2O2 is dissociated into O2 by catalase. The red ball is 16O on quartz surface, and the pink ball is 18O that derives from H218O. For detail equations, see

SI Appendix, Table S7

.

References

    1. Ślesak I., Ślesak H., Kruk J., Oxygen and hydrogen peroxide in the early evolution of life on Earth: In silico comparative analysis of biochemical pathways. Astrobiology 12, 775–784 (2012). -PMC -PubMed
    1. Inupakutika M. A., Sengupta S., Devireddy A. R., Azad R. K., Mittler R., The evolution of reactive oxygen species metabolism. J. Exp. Bot. 67, 5933–5943 (2016). -PubMed
    1. Jabłońska J., Tawfik D. S., The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation. Nat. Ecol. Evol. 5, 442–448 (2021). -PubMed
    1. Taverne Y. J., Caron A., Diamond C., Fournier G., Lyons T. W., “Oxidative stress and the early coevolution of life and biospheric oxygen” in Oxidative Stress (Elsevier, 2020), pp. 67–85.
    1. Farquhar J., Bao H., Thiemens M., Atmospheric influence of Earth’s earliest sulfur cycle. Science 289, 756–758 (2000). -PubMed

Grants and funding

LinkOut - more resources