Manganese-oxidizing photosynthesis before the rise of cyanobacteria
Open accessAbstract
The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O2--multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redox-sensitive detrital grains--reveal that the original Mn-oxide phases were not produced by reactions with O2, which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.
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The interpretation of sediment manganese enrichments is robust regardless of the possibility of oxygen-free manganese oxidation through UV photooxidation, photosynthetic oxidation, or oxidation with elemental sulfur, given rapid manganese reduction under anoxic conditions.
“This interpretation of sediment manganese enrichments is robust regardless of the possibility of oxygen-free manganese oxidation-through UV photooxidation (Anbar & Holland 1992), photosynthetic oxidation ( Johnson et al. 2013), or oxidation with elemental sulfur (Daye et al. 2019)-given rapid manganese reduction under anoxic conditions (e.g., Busigny et al. 2014).”
From The History of Ocean Oxygenation (2022) · cites this paper as Johnson et al. 2013
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- Authors
- Johnson, J. E., Webb, S. M., Thomas, K., Ono, S., Kirschvink, J. L., & Fischer, W. W.
- Affiliations
- California Institute of Technology (US)
- Stanford Synchrotron Radiation Lightsource (US)
- Massachusetts Institute of Technology (US)
- Tokyo Institute of Technology (JP)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-06-24
- Volume
- 110
- Issue
- 28
- Pages
- 11238-11243
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3710856
- OpenAlex
- W2103118098
- Cited by
- 238
- References
- 62
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 24 · 2023: 22 · 2022: 19 · 2021: 20 · 2020: 21 · 2019: 25 · 2018: 16 · 2017: 17 · 2016: 15 · 2015: 13 · 2014: 19 · 2013: 5
- FWCI
- 11.79
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation
- David and Lucile Packard Foundation
- U.S. Department of Energy
- National Aeronautics and Space Administration
- Agouron Institute
- Office of Science
- SLAC National Accelerator Laboratory
- Topics
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Physical Sciences › Earth and Planetary Sciences › Geochemistry and Petrology › Geochemistry and Elemental Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- manganese cycle, oxygen-evolving complex, Paleoproterozoic, manganese oxide, carbonate minerals, diagenesis, sulfur isotopes, carbon isotopes
- MeSH terms
- Cyanobacteria, Manganese, Oxidation-Reduction, Photosynthesis, Biomarkers
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