Manganese-oxidizing photosynthesis before the rise of cyanobacteria

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 obt...

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Main Authors: Thomas, Katherine, Ono, Shuhei, Johnson, Jena E., Webb, Samuel M., Kirschvink, Joseph L., Fischer, Woodward W.
Other Authors: Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2014
Online Access:http://hdl.handle.net/1721.1/85597
https://orcid.org/0000-0002-1348-9584
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author Thomas, Katherine
Ono, Shuhei
Johnson, Jena E.
Webb, Samuel M.
Kirschvink, Joseph L.
Fischer, Woodward W.
author2 Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
author_facet Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Thomas, Katherine
Ono, Shuhei
Johnson, Jena E.
Webb, Samuel M.
Kirschvink, Joseph L.
Fischer, Woodward W.
author_sort Thomas, Katherine
collection MIT
description 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 O[subscript 2]—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 O[subscript 2], 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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spelling mit-1721.1/855972022-10-02T02:48:33Z Manganese-oxidizing photosynthesis before the rise of cyanobacteria Thomas, Katherine Ono, Shuhei Johnson, Jena E. Webb, Samuel M. Kirschvink, Joseph L. Fischer, Woodward W. Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Thomas, Katherine Ono, Shuhei 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 O[subscript 2]—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 O[subscript 2], 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. Agouron Institute 2014-03-10T20:00:10Z 2014-03-10T20:00:10Z 2013-06 2013-03 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/85597 Johnson, J. E., S. M. Webb, K. Thomas, S. Ono, J. L. Kirschvink, and W. W. Fischer. “Manganese-Oxidizing Photosynthesis before the Rise of Cyanobacteria.” Proceedings of the National Academy of Sciences 110, no. 28 (July 9, 2013): 11238–11243. https://orcid.org/0000-0002-1348-9584 en_US http://dx.doi.org/10.1073/pnas.1305530110 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS
spellingShingle Thomas, Katherine
Ono, Shuhei
Johnson, Jena E.
Webb, Samuel M.
Kirschvink, Joseph L.
Fischer, Woodward W.
Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title_full Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title_fullStr Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title_full_unstemmed Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title_short Manganese-oxidizing photosynthesis before the rise of cyanobacteria
title_sort manganese oxidizing photosynthesis before the rise of cyanobacteria
url http://hdl.handle.net/1721.1/85597
https://orcid.org/0000-0002-1348-9584
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