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Dark oxygen

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Dark oxygen production refers to the generation of molecular oxygen (O2) through processes that do not involve light-dependent oxygenic photosynthesis. The name therefore uses a different sense of 'dark' than that used in the phrase "biological dark matter" (for example) which indicates obscurity to scientific assessment rather than the photometric meaning. While the majority of Earth's oxygen is produced by plants and photosynthetically active microorganisms via photosynthesis, dark oxygen production occurs via a variety of abiotic and biotic processes and may support aerobic metabolism in dark, anoxic environments.

Abiotic production

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Abiotic production of dark oxygen can occur through several mechanisms, such as:

  • Water radiolysis: This process typically takes place in dark geological ecosystems, such as aquifers, where the decay of radioactive elements in surrounding rock leads to the breakdown of water molecules, producing O2.[1]
  • Oxidation of surface-bound radicals: On silicon-bearing minerals like quartz, surface-bound radicals can undergo oxidation, contributing to O2 production.[2][3][4]

In addition to direct O2 formation, these processes often produce reactive oxygen species (ROS), such as hydroxyl radicals (OH•), superoxide (O2•-), and hydrogen peroxide (H2O2). These ROS can be converted into O2 and water either biotically, through enzymes like superoxide dismutase and catalase, or abiotically, via reactions with ferrous iron and other reduced metals.[5][6]

Biotic production

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Biotic production of dark oxygen is performed by microorganisms through distinct microbial processes, including:

  • Chlorite dismutation: This involves the dismutation of chlorite (ClO2-) into O2 and chloride ions.[7]
  • Nitric oxide dismutation: This involves the dismutation of nitric oxide (NO) into O2 and dinitrogen gas (N2) or nitrous oxide (N2O). [8][9][10]
  • Water lysis via methanobactins: Methanobactins can lyse water molecules to produce O2.[11]

These processes enable microbial communities to sustain aerobic metabolism in environments that lack oxygen.

Experimental evidence

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Recent studies have provided evidence for dark oxygen production in various geological and subsurface environments:

  • Groundwater ecosystems: Dissolved oxygen concentrations have been measured in old groundwaters previously assumed to be anoxic. The presence of O2 is attributed to microbial communities capable of producing dark oxygen and water radiolysis. Metagenomic analyses and oxygen isotope studies further support local oxygen generation rather than atmospheric mixing.[12]
    A bed of manganese nodules offshore of the Cook Islands
  • Seafloor environments: A study on manganese nodules on the abyssal seafloor has suggested abiotic dark oxygen production.[13] The proposed mechanism is electrolysis, because voltages were recorded on the surface of the nodules. However, no voltage great enough to split water was measured, the energy source for electrolysis is unknown, and previous experiments from the same region have not found any evidence of oxygen production.[14][15][16][17][18]

Implications

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Despite its diverse pathways, dark oxygen production has traditionally been considered negligible in Earth's systems. Recent evidence suggests that O2 is produced and consumed in dark, apparently anoxic environments on a much larger scale than previously thought, with implications for global biogeochemical cycles.[19][20]

References

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  1. ^ Das, Soumya (2013). "Critical Review of Water Radiolysis Processes, Dissociation Products, and Possible Impacts on the Local Environment: A Geochemist". Australian Journal of Chemistry. 66 (5): 522. doi:10.1071/CH13012. ISSN 0004-9425.
  2. ^ He, Hongping; Wu, Xiao; Xian, Haiyang; Zhu, Jianxi; Yang, Yiping; Lv, Ying; Li, Yiliang; Konhauser, Kurt O. (2021-11-16). "An abiotic source of Archean hydrogen peroxide and oxygen that pre-dates oxygenic photosynthesis". Nature Communications. 12 (1): 6611. Bibcode:2021NatCo..12.6611H. doi:10.1038/s41467-021-26916-2. ISSN 2041-1723. PMC 8595356. PMID 34785682.
  3. ^ He, Hongping; Wu, Xiao; Zhu, Jianxi; Lin, Mang; Lv, Ying; Xian, Haiyang; Yang, Yiping; Lin, Xiaoju; Li, Shan; Li, Yiliang; Teng, H. Henry; Thiemens, Mark H. (2023-03-28). "A mineral-based origin of Earth's initial hydrogen peroxide and molecular oxygen". Proceedings of the National Academy of Sciences. 120 (13): e2221984120. Bibcode:2023PNAS..12021984H. doi:10.1073/pnas.2221984120. ISSN 0027-8424. PMC 10068795. PMID 36940327.
  4. ^ Stone, Jordan; Edgar, John O.; Gould, Jamie A.; Telling, Jon (2022-08-08). "Tectonically-driven oxidant production in the hot biosphere". Nature Communications. 13 (1): 4529. Bibcode:2022NatCo..13.4529S. doi:10.1038/s41467-022-32129-y. ISSN 2041-1723. PMC 9360021. PMID 35941147.
  5. ^ Sutherland, Kevin M.; Hemingway, Jordon D.; Johnston, David T. (May 2022). "The influence of reactive oxygen species on "respiration" isotope effects". Geochimica et Cosmochimica Acta. 324: 86–101. Bibcode:2022GeCoA.324...86S. doi:10.1016/j.gca.2022.02.033.
  6. ^ Xu, Jie; Sahai, Nita; Eggleston, Carrick M.; Schoonen, Martin A.A. (February 2013). "Reactive oxygen species at the oxide/water interface: Formation mechanisms and implications for prebiotic chemistry and the origin of life". Earth and Planetary Science Letters. 363: 156–167. Bibcode:2013E&PSL.363..156X. doi:10.1016/j.epsl.2012.12.008.
  7. ^ Xu, Jianlin; Logan, Bruce E. (August 2003). "Measurement of chlorite dismutase activities in perchlorate respiring bacteria". Journal of Microbiological Methods. 54 (2): 239–247. doi:10.1016/S0167-7012(03)00058-7. PMID 12782379.
  8. ^ Ettwig, Katharina F.; Speth, Daan R.; Reimann, Joachim; Wu, Ming L.; Jetten, Mike S. M.; Keltjens, Jan T. (2012). "Bacterial oxygen production in the dark". Frontiers in Microbiology. 3: 273. doi:10.3389/fmicb.2012.00273. ISSN 1664-302X. PMC 3413370. PMID 22891064.
  9. ^ Kraft, Beate; Jehmlich, Nico; Larsen, Morten; Bristow, Laura A.; Könneke, Martin; Thamdrup, Bo; Canfield, Donald E. (2022-01-07). "Oxygen and nitrogen production by an ammonia-oxidizing archaeon". Science. 375 (6576): 97–100. Bibcode:2022Sci...375...97K. doi:10.1126/science.abe6733. ISSN 0036-8075. PMID 34990242.
  10. ^ Murali, Ranjani; Pace, Laura A.; Sanford, Robert A.; Ward, L. M.; Lynes, Mackenzie M.; Hatzenpichler, Roland; Lingappa, Usha F.; Fischer, Woodward W.; Gennis, Robert B.; Hemp, James (2024-06-25). "Diversity and evolution of nitric oxide reduction in bacteria and archaea". Proceedings of the National Academy of Sciences. 121 (26): e2316422121. Bibcode:2024PNAS..12116422M. doi:10.1073/pnas.2316422121. ISSN 0027-8424. PMC 11214002. PMID 38900790.
  11. ^ Dershwitz, Philip; Bandow, Nathan L.; Yang, Junwon; Semrau, Jeremy D.; McEllistrem, Marcus T.; Heinze, Rafael A.; Fonseca, Matheus; Ledesma, Joshua C.; Jennett, Jacob R.; DiSpirito, Ana M.; Athwal, Navjot S.; Hargrove, Mark S.; Bobik, Thomas A.; Zischka, Hans; DiSpirito, Alan A. (2021-06-25). Parales, Rebecca E. (ed.). "Oxygen Generation via Water Splitting by a Novel Biogenic Metal Ion-Binding Compound". Applied and Environmental Microbiology. 87 (14): e0028621. Bibcode:2021ApEnM..87E.286D. doi:10.1128/AEM.00286-21. ISSN 0099-2240. PMC 8231713. PMID 33962982.
  12. ^ Ruff, S. Emil; Humez, Pauline; de Angelis, Isabella Hrabe; Diao, Muhe; Nightingale, Michael; Cho, Sara; Connors, Liam; Kuloyo, Olukayode O.; Seltzer, Alan; Bowman, Samuel; Wankel, Scott D.; McClain, Cynthia N.; Mayer, Bernhard; Strous, Marc (2023-06-13). "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems". Nature Communications. 14 (1): 3194. Bibcode:2023NatCo..14.3194R. doi:10.1038/s41467-023-38523-4. ISSN 2041-1723. PMC 10264387. PMID 37311764.
  13. ^ Sweetman, Andrew K.; Smith, Alycia J.; de Jonge, Danielle S. W.; Hahn, Tobias; Schroedl, Peter; Silverstein, Michael; Andrade, Claire; Edwards, R. Lawrence; Lough, Alastair J. M.; Woulds, Clare; Homoky, William B.; Koschinsky, Andrea; Fuchs, Sebastian; Kuhn, Thomas; Geiger, Franz (August 2024). "Evidence of dark oxygen production at the abyssal seafloor". Nature Geoscience. 17 (8): 737–739. doi:10.1038/s41561-024-01480-8. ISSN 1752-0894.
  14. ^ Smith, K. L.; Laver, M. B.; Brown, N. O. (1983). "Sediment community oxygen consumption and nutrient exchange in the central and eastern North Pacific1". Limnology and Oceanography. 28 (5): 882–898. doi:10.4319/lo.1983.28.5.0882. ISSN 0024-3590.
  15. ^ Khripounoff, Alexis; Caprais, Jean-Claude; Crassous, Philippe; Etoubleau, Joël (2006). "Geochemical and biological recovery of the disturbed seafloor in polymetallic nodule fields of the Clipperton-Clarion Fracture Zone (CCFZ) at 5,000-m depth". Limnology and Oceanography. 51 (5): 2033–2041. doi:10.4319/lo.2006.51.5.2033.
  16. ^ Vonnahme, T. R.; Molari, M.; Janssen, F.; Wenzhöfer, F.; Haeckel, M.; Titschack, J.; Boetius, A. (2020). "Effects of a deep-sea mining experiment on seafloor microbial communities and functions after 26 years". Science Advances. 6 (18). doi:10.1126/sciadv.aaz5922. ISSN 2375-2548. PMC 7190355. PMID 32426478.
  17. ^ Stratmann, Tanja; Voorsmit, Ilja; Gebruk, Andrey; Brown, Alastair; Purser, Autun; Marcon, Yann; Sweetman, Andrew K.; Jones, Daniel O. B.; van Oevelen, Dick (2018). "Recovery of Holothuroidea population density, community composition, and respiration activity after a deep‐sea disturbance experiment". Limnology and Oceanography. 63 (5): 2140–2153. doi:10.1002/lno.10929. ISSN 0024-3590.
  18. ^ An, Sung-Uk; Baek, Ju-Wook; Kim, Sung-Han; Baek, Hyun-Min; Lee, Jae Seong; Kim, Kyung-Tae; Kim, Kyeong Hong; Hyeong, Kiseong; Chi, Sang-Bum; Park, Chan Hong (2024). "Regional differences in sediment oxygen uptake rates in polymetallic nodule and co-rich polymetallic crust mining areas of the Pacific Ocean". Deep Sea Research Part I: Oceanographic Research Papers. 207: 104295. doi:10.1016/j.dsr.2024.104295. ISSN 0967-0637.
  19. ^ Sweetman, Andrew K.; Smith, Alycia J.; de Jonge, Danielle S. W.; Hahn, Tobias; Schroedl, Peter; Silverstein, Michael; Andrade, Claire; Edwards, R. Lawrence; Lough, Alastair J. M.; Woulds, Clare; Homoky, William B.; Koschinsky, Andrea; Fuchs, Sebastian; Kuhn, Thomas; Geiger, Franz (August 2024). "Evidence of dark oxygen production at the abyssal seafloor". Nature Geoscience. 17 (8): 737–739. doi:10.1038/s41561-024-01480-8. ISSN 1752-0894.
  20. ^ Ruff, S. Emil; Humez, Pauline; de Angelis, Isabella Hrabe; Diao, Muhe; Nightingale, Michael; Cho, Sara; Connors, Liam; Kuloyo, Olukayode O.; Seltzer, Alan; Bowman, Samuel; Wankel, Scott D.; McClain, Cynthia N.; Mayer, Bernhard; Strous, Marc (2023-06-13). "Hydrogen and dark oxygen drive microbial productivity in diverse groundwater ecosystems". Nature Communications. 14 (1). doi:10.1038/s41467-023-38523-4. ISSN 2041-1723. PMC 10264387. PMID 37311764.
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