The Mesoproterozoic era (1,600–1,000 million years ago (Ma)) has long been considered a period of relative environmental stasis, with persistently low levels of atmospheric oxygen. There remains much uncertainty, however, over the evolution of ocean chemistry during this period, which may have been of profound significance for the early evolution of eukaryotic life. Here we present rare earth element, iron-speciation and inorganic carbon isotope data to investigate the redox evolution of the 1,600–1,550 Ma Yanliao Basin, North China Craton. These data confirm that the ocean at the start of the Mesoproterozoic was dominantly anoxic and ferruginous. Significantly, however, we find evidence for a progressive oxygenation event starting at ~1,570 Ma, immediately prior to the occurrence of complex multicellular eukaryotes in shelf areas of the Yanliao Basin. Our study thus demonstrates that oxygenation of the Mesoproterozoic environment was far more dynamic and intense than previously envisaged, and establishes an important link between rising oxygen and the emerging record of diverse, multicellular eukaryotic life in the early Mesoproterozoic.
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Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008).
Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Philos. Trans. R. Soc. Lond. B 361, 1023–1038 (2006).
Agić, H., Moczydłowska, M. & Yin, L. Diversity of organic-walled microfossils from the early Mesoproterozoic Ruyang Group, North China Craton—a window into the early eukaryote evolution. Precambrian Res. 297, 101–130 (2017).
Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66–69 (2001).
Vorob’eva, N. G., Sergeev, V. N. & Petrov, P. Y. Kotuikan Formation assemblage: a diverse organic-walled microbiota in the Mesoproterozoic Anabar succession, northern Siberia. Precambrian Res. 256, 201–222 (2015).
Zhu, S. et al. Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China. Nat. Commun. 7, 11500 (2016).
Summons, R. E., Bradley, A. S., Jahnke, L. L. & Waldbauer, J. R. Steroids, triterpenoids and molecular oxygen. Philos. Trans. R. Soc. Lond. B 361, 951–968 (2006).
Lyons, T. W., Reinhard, C. T. & Planavsky, N. J. The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315 (2014).
Planavsky, N. J. et al. Low Mid-Proterozoic atmospheric oxygen levels and the delayed rise of animals. Science 346, 635–638 (2014).
Zhang, S. et al. Sufficient oxygen for animal respiration 1,400 million years ago. Proc. Natl Acad. Sci. USA 113, 1731–1736 (2016).
Daines, S. J., Mills, B. J. & Lenton, T. M. Atmospheric oxygen regulation at low Proterozoic levels by incomplete oxidative weathering of sedimentary organic carbon. Nat. Commun. 8, 14379 (2017).
Poulton, S. W., Fralick, P. W. & Canfield, D. E. Spatial variability in oceanic redox structure 1.8 billion years ago. Nat. Geosci. 3, 486–490 (2010).
Planavsky, N. J. et al. Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477, 448–451 (2011).
Poulton, S. W. & Canfield, D. E. Ferruginous conditions: a dominant feature of the ocean through Earth’s history. Elements 7, 107–112 (2011).
Wang, X. et al. Oxygen, climate and the chemical evolution of a 1400 million year old tropical marine setting. Am. J. Sci. 317, 861–900 (2017).
Sperling, E. A. et al. Redox heterogeneity of subsurface waters in the Mesoproterozoic ocean. Geobiology 12, 373–386 (2014).
Luo, G. et al. Shallow stratification prevailed for ~1700 to ~1300 Ma ocean: evidence from organic carbon isotopes in the North China Craton. Earth Planet. Sci. Lett. 400, 219–232 (2014).
Tang, D., Shi, X., Wang, X. & Jiang, G. Extremely low oxygen concentration in mid-Proterozoic shallow seawaters. Precambrian Res. 276, 145–157 (2016).
Guo, H. et al. Sulfur isotope composition of carbonate-associated sulfate from the Mesoproterozoic Jixian Group, North China: implications for the marine sulfur cycle. Precambrian Res. 266, 319–336 (2015).
Mei, M. Preliminary study on sequence-stratigraphic position and origin for molar-tooth structure of the Gaoyuzhuang Formation of Mesoproterozoic at Jixian section in Tianjin. J. Palaeogeogr. 7, 437–447 (2005).
Tian, H. et al. Zircon LA-MC-ICPMS U–Pb dating of tuff from Mesoproterozoic Gaoyuzhuang Formation in Jixian Country of North China and its geological significance. Acta Geosci. Sin. 36, 647–658 (2015).
Li, H. et al. Further constraints on the new subdivision of the Mesoproterozoic stratigraphy in the northern North China Craton. Acta Petrol. Sin. 26, 2131–2140 (2010).
Michard, A., Albarède, F., Michard, G., Minster, J. F. & Charlou, J. L. Rare-earth elements and uranium in high-temperature solutions from East Pacific Rise hydrothermal vent field (13 °N). Nature 303, 795–797 (1983).
Sholkovitz, E. R., Landing, W. M. & Lewis, B. L. Ocean particle chemistry: the fractionation of rare earth elements between suspended particles and seawater. Geochim. Cosmochim. Acta. 58, 1567–1579 (1994).
Cantrell, K. J. & Byrne, R. H. Rare earth element complexation by carbonate and oxalate ions. Geochim. Cosmochim. Acta. 51, 597–605 (1987).
Bau, M. Controls on the fractionation of isovalent trace elements in magmatic and aqueous systems: evidence from Y/Ho, Zr/Hf, and lanthanide tetrad effect. Contrib. Mineral. Petrol. 123, 323–333 (1996).
Nozaki, Y., Zhang, J. & Amakawa, H. The fractionation between Y and Ho in marine environment. Earth Planet. Sci. Lett. 148, 329–340 (1997).
Bau, M. & Koschinsky, A. Oxidative scavenging of cerium on hydrous Fe oxides: evidence from the distribution of rare earth elements and yttrium between Fe oxides and Mn oxides in hydrogenetic ferromanganese crusts. Geochem. J. 43, 37–47 (2009).
German, C. R., Holliday, B. P. & Elderfield, H. Redox cycling of rare earth elements in the suboxic zone of the Black Sea. Geochim. Cosmochim. Acta. 55, 3553–3558 (1991).
Bau, M., Moller, P. & Dulski, P. Yttrium and lanthanides in eastern Mediterranean seawater and their fractionation during redox-cycling. Mar. Chem. 56, 123–131 (1997).
Tostevin, R. et al. Low-oxygen waters limited habitable space for early animals. Nat. Commun. 7, 12818 (2016).
Nothdurft, L. D., Webb, G. E. & Kamber, B. S. Rare earth element geochemistry of Late Devonian reefal carbonates, Canning Basin, Western Australia: confirmation of a seawater REE proxy in ancient limestones. Geochim. Cosmochim. Acta. 68, 263–283 (2004).
Banner, J. L., Hanson, G. N. & Meyers, W. J. Rare earth elements and Nd isotopic variations in regionally extensive dolomites from the Burlington–Keokuk Formation (Mississippian): implications for REE mobility during carbonate diagenesis. J. Sediment. Petrol. 58, 415–432 (1988).
Zhang, K., Zhu, X. & Yan, B. A refined dissolution method for rare earth element studies of bulk carbonate rocks. Chem. Geol. 412, 82–91 (2015).
Poulton, S. W., Frallck, P. W. & Canfield, D. E. The transition to a sulphidic ocean ~1.84 billion years ago. Nature 431, 173–177 (2004).
Clarkson, M. O. et al. Dynamic anoxic ferruginous conditions during the end-Permian mass extinction and recovery. Nat. Commun. 7, 12236 (2016).
Wood, R. A. et al. Dynamic redox conditions control late Ediacaran metazoan ecosystems in the Nama Group, Namibia. Precambrian Res. 261, 252–271 (2015).
Clarkson, M. O., Poulton, S. W., Guilbaud, R. & Wood, R. A. Assessing the utility of Fe/Al and Fe-speciation to record water column redox conditions in carbonate-rich sediments. Chem. Geol. 382, 111–122 (2014).
Poulton, S. W. & Canfield, D. E. Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates. Chem. Geol. 214, 209–221 (2005).
Poulton, S. W. & Raiswell, R. The low-temperature geochemical cycle of iron: from continental fluxes to marine sediment deposition. Am. J. Sci. 302, 774–805 (2002).
Raiswell, R. & Canfield, D. E. Sources of iron for pyrite formation in marine sediments. Am. J. Sci. 298, 219–245 (1998).
Ling, H. et al. Cerium anomaly variations in Ediacaran–earliest Cambrian carbonates from the Yangtze Gorges area, South China: implications for oxygenation of coeval shallow seawater. Precambrian Res. 225, 110–127 (2013).
Li, R., Chen, J., Zang, S. & Chen, Z. Secular variations in carbon isotopic compositions of carbonates from Proterozoic successions in the Ming Tombs Section of the North China Platform. J. Asian Earth Sci. 22, 329–341 (2003).
Guo, H. et al. Isotopic composition of organic and inorganic carbon from the Mesoproterozoic Jixian Group, North China: implications for biological and oceanic evolution. Precambrian Res. 224, 169–183 (2013).
Canfield, D. E., Raiswell, R., Westrich, J. T., Reaves, C. M. & Berner, R. A. The use of chromium reduction in the analysis of reduced inorganic sulfur in sediments and shales. Chem. Geol. 54, 149–155 (1986).
This work was supported by NSFC Grant 41430104 and CAGS Research Fund YYWF201603 to X.K.Z., a China Scholarship Council award to K.Z. and a China Geological Survey Grant DD20160120-04 to B. Yan. S.W.P. acknowledges support from a Royal Society Wolfson Research Merit Award. We thank L. Gao and P. Liu for field guidance, and F. Shi, C. Tang, X. Peng, C. Pan, N. Zhao, C. Bao, Z. Zhou, F. Zhang and Y. Guo for field-work assistance. We acknowledge F. Xu and M. Lv for assistance in the elemental analysis, Y. Xiong for help with the Fe-speciation experiments, Y. Shen, K. Chen and W. Huang for carbon isotope analyses and F. Bowyer for assistance with cathodoluminescence. We also express our thanks to J. Li, D. Li, Y. He, J. Ma, X. Zou and K. Du for logistical support.
The authors declare no competing interests.
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Zhang, K., Zhu, X., Wood, R.A. et al. Oxygenation of the Mesoproterozoic ocean and the evolution of complex eukaryotes. Nature Geosci 11, 345–350 (2018). https://doi.org/10.1038/s41561-018-0111-y
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