Earth and Planetary Science Letters 527 (2019) 115797

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Earth and Planetary Science Letters

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A pulse of oxygen increase in the early Mesoproterozoic ocean at ca. 1.57–1.56 Ga ∗ ∗ Mohan Shang a,b, Dongjie Tang a,c, , Xiaoying Shi a,b, , Limin Zhou d, Xiqiang Zhou e, Huyue Song f, Ganqing Jiang g a State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Beijing), Beijing 100083, China b School of Earth Sciences and Resources, China University of Geosciences (Beijing), Beijing 100083, China c Institute of Earth Sciences, China University of Geosciences (Beijing), Beijing 100083, China d National Research Center of Geoanalysis, Beijing 100037, China e Key Lab of Petroleum Resources Research, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China f State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences (Wuhan), Wuhan 430074, China g Department of Geoscience, University of Nevada, Las Vegas, NV 89154-4010, USA a r t i c l e i n f o a b s t r a c t

Article history: The relationship between oxygen and evolution of early eukaryotes including algae and primitive animals Received 2 January 2019 in geological history has been debated, partly due to the varying estimates of oxygen levels in the mid- Received in revised form 25 July 2019 Proterozoic (ca. 1.8–0.8 Ga) ocean and atmosphere. The upper part of the Gaoyuzhuang Formation (ca. Accepted 29 August 2019 1.60–1.54 Ga) in North China hosts decimeter-scale multicellular eukaryotic fossils and is documented Available online xxxx with a decrease in cerium anomaly indicative of ocean oxygenation. However, the atmospheric oxygen Editor: I. Halevy level across this interval and its subsequent oxidation state require further investigation using additional + 13 13 Keywords: redox proxies. Here we report I/(Ca Mg) ratios, carbonate/organic carbon isotopes (δ Ccarb and δ Corg), boring billion and phosphorous (P) contents across the ca. 1.57–1.56 Ga fossil-bearing interval in the North China oxygenation episode Platform. High I/(Ca+Mg) ratios (≥2.6 μmol/mol; up to 3.8 μmol/mol) from shallow-water carbonates Gaoyuzhuang Formation of the Gaoyuzhuang Formation suggest an episode of significant oxygen increase up to ≥4% PAL (present + I/(Ca Mg) atmospheric level). The I/(Ca+Mg) ratios return back to ≤0.5 μmol/mol shortly after the peak values North China Platform without evidence for increasing water depth or diagenetic alteration, implying a short-lived oxidation 13 13 event. The increase of I/(Ca+Mg) ratios is associated with a −3.5h negative δ Ccarb and δ Corg anomaly and an increase in P/Al ratios that are best explained by oxidation of dissolved organic carbon (DOC) in the ocean. Oxygen consumption through oxidation of DOC may have quickly lowered marine and atmospheric O2 levels to the early mid-Proterozoic (1.8–1.4 Ga) background oxygen concentration of ≤0.1–1% PAL. Short-lived oxidation events in an overall anoxic mid-Proterozoic ocean and atmosphere best explain the existing geochemical data and evolutionary stasis of eukaryotes during the “Boring Billion”. © 2019 Elsevier B.V. All rights reserved.

1. Introduction basins at ca. 1.85 Ga (Planavsky et al., 2018a), ca. 1.57–1.54 Ga (Tang et al., 2016; Zhang et al., 2018), ca. 1.4 Ga (Cox et The mid-Proterozoic (ca. 1.8–0.8 Ga) witnessed the emergence al., 2016; Hardisty et al., 2017;Mukherjee and Large, 2016; but slow diversification of eukaryotes (Butterfield, 2015; Knoll, Sperling et al., 2014; Yang et al., 2017; Zhang et al., 2016), and 2014). Multi-proxy geochemical studies suggested that the mid- ca. 1.1 Ga (Gilleaudeau et al., 2016). The overall weakly oxy- Proterozoic ocean was mostly ferruginous with euxinic wedges genated condition was possibly caused by low primary produc- on shelf margins (e.g., Luo et al., 2014; Planavsky et al., 2011; tion and low organic carbon burial flux (Crockford et al., 2018; Poulton and Canfield, 2011) and perhaps episodes of increased Ozaki et al., 2019). Estimates of mid-Proterozoic atmospheric O2 oxygen or spatially-limited oxygenation in some sedimentary levels also vary significantly. Earlier assessments on the basis of iron retention in paleosols suggested atmospheric O2 con- centrations of ≥1–3% PAL [present atmospheric levels] (Rye and * Corresponding authors at: State Key Laboratory of Biogeology and Environmen- tal Geology, China University of Geosciences (Beijing), Beijing 100083, China. Holland, 1998;Zbinden et al., 1988; but see Planavsky et al., E-mail addresses: [email protected] (D. Tang), [email protected] (X. Shi). 2018b for a different view). Paleoenvironment and diagenetic mod- https://doi.org/10.1016/j.epsl.2019.115797 0012-821X/© 2019 Elsevier B.V. All rights reserved. 2 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 els constructed from trace element concentrations, organic car- have been interpreted as deposits from shallow subtidal to in- bon contents and biomarkers of the Mesoproterozoic Xiamaling tertidal environments (Mei, 2008). Member II consists of man- Formation (ca. 1.40–1.35 Ga) in North China also suggested at- ganiferous dolostone in the lower part and medium- to thick- mospheric O2 levels of ≥4–8% PAL (Zhang et al., 2016, 2017). bedded dolostone in the upper part. The lower Member II con- However, the lack of observable chromium (Cr) isotope fraction- tains dark shale interbeds with manganese concretions and has ation in mid-Proterozoic marine ironstones and shales, and Ce been interpreted as subtidal deposits (Mei, 2008). The upper Mem- anomalies in carbonates implies a much lower O2 level that was ber II contains microbially induced sedimentary structures and likely <0.1–1% PAL (Bellefroid et al., 2018;Cole et al., 2016; mud cracks indicative of deposition from intertidal to suprati- Planavsky et al., 2014). In contrast, Cr isotopes from the 1.1–0.9 Ga dal environments (Fig. 2B). The lower to middle part of Mem- marine carbonates show considerable fractionations and suggest ber III is composed of thin-bedded muddy dolostone (Fig. 2C and atmospheric O2 concentrations of >0.1–1% PAL (Gilleaudeau et al., D), calcareous mudstone with cm- to dm-sized carbonate concre- 2016). Similarly, high Cr isotopes from the Shennongjia Group in tions (Fig. 2E) and some thrombolite layers (Fig. 2F). The gen- South China suggest atmospheric O2 levels of >1% PAL since ca. eral lack of wave- and tide-agitated sedimentary structures in 1.33 Ga (Canfield et al., 2018). this part suggests deposition in low-energy environments proba- The higher O2 estimates for mid-Proterozoic surface environ- bly close to storm wave base (Guo et al., 2013;Luo et al., 2014; ments would argue against oxygen limitation as an evolutionary Mei, 2008), while the layered thrombolites were likely formed barrier for eukaryotes (particularly animals) because many early in subtidal environments (Tang et al., 2013). The upper part of stem-group animals and sponges have a minimum oxygen require- Member III consists of laminated microbial dolostones with flaser ment of 0.5–4% PAL (e.g., Mills et al., 2014;Sperling et al., 2013; bedding (Fig. 2G) and interference ripple marks, suggestive of de- Zhang et al., 2016). However, most geochemical data used for position from shallow subtidal to intertidal environments. Member O2 estimation were obtained from short stratigraphic intervals in IV of the Gaoyuzhuang Formation is characterized by massive mi- geographically distinct sedimentary basins, which leads to uncer- crobial reef dolostones with a total thickness up to 450 m (Mei, tainties about the stability of O2 levels in the mid-Proterozoic. 2008). Conical stromatolites (Conophyton-like) over 2 m high and Although many have assumed that atmospheric O2 concentrations 35 cm wide and various other microbialites (cf. Bartley et al., 2015) remained relatively stable in the mid-Proterozoic, either at lower are common in this member, suggesting subtidal depositional en- or higher levels (e.g., Lyons et al., 2014; Planavsky et al., 2014; vironments at least episodically below fair-weather wave base. Pre- Zhang et al., 2016), there exists a possibility that O2 concentra- vious studies on carbonate fabrics and mineral compositions of the tions fluctuated significantly during the mid-Proterozoic. Gaoyuzhuang Formation suggested fabric-retentive early dolomiti- A particularly intriguing interval to test the oxygen stability zation (e.g., Zhang W. et al., 2016; Tang et al., 2017a), which may is the ca. 1.57–1.56 Ga oxidation event documented from the have helped preserve primary geochemical signatures. Gaoyuzhuang Formation of the North China Platform (Zhang et al., 2018). This interval hosts decimeter-scale multicellular eu- 3. Materials and methods karyotes (Zhu et al., 2016) that have been linked to oxygen increase in the early Mesoproterozoic. The associated decrease of cerium (Ce) anomaly from ∼1.0 to ∼0.8 was interpreted as In this study, 234 samples from Member II and III of the evidence for significant ocean oxygenation (Tang et al., 2016; Gaoyuzhuang Formation in the Gan’gou section were analyzed. Zhang et al., 2018), but whether it represents a pulse of oxy- Decimeter-sized multicellular eukaryotic fossils were not reported gen increase or the initiation of a permanently more oxygenated in this section, but the lithological and carbon isotope correlation Mesoproterozoic ocean requires further investigation. In this pa- indicates that the studied interval covers the fossil-bearing strata per, we report iodine-to-calcium-magnesium [I/(Ca+Mg)] ratios of of the Qianxi and Kuancheng sections (Zhu et al., 2016). The sam- 13 pling section is well exposed along the fresh road cuts at Gan’gou carbonate rocks, carbonate/organic carbon isotopes (δ Ccarb and ◦   ◦   13 (40 39 35.05 N, 116 14 35.63 E), north of Beijing, China (Fig. 1). δ Corg), and phosphorus contents across the ca. 1.57–1.56 Ga in- terval of the Gaoyuzhuang Formation and discuss the potential Collected samples were cut into chips and only the central parts temporal changes in atmospheric oxygen concentration during the of the samples were used for geochemical analyses. Fresh sample ∼ early Mesoproterozoic. chips were cleaned, dried, and then grounded into powders ( 200 meshes) in an agate mortar avoiding any metal contact. 2. Geological setting Macroscopic features were observed in the field. Microfabrics were examined on thin sections with a Stereo Discovery V20 mi- Our study focuses on the carbonate rocks from Member II and croscope for large scope and a Zeiss Axio Scope A1 microscope III of the Gaoyuzhuang Formation in the Mesoproterozoic North for high magnification. Ultrastructures were investigated using a China Platform (Fig. 1). The Gaoyuzhuang Formation is the basal Zeiss Supra 55 field emission scanning electron microscope (FE- unit of the Jixian Group that overlies the Dahongyu Formation SEM) under 20 kV accelerating voltage with a working distance of of the Changcheng Group and underlies the Yangzhuang Forma- ∼15 mm, at the State Key Laboratory of Biogeology and Environ- tion of the Jixian Group (Fig. 1D). The Gaoyuzhuang Formation is mental Geology, China University of Geosciences (Beijing) (CUGB). commonly interpreted as being deposited in a shelf environment Secondary electron imaging detector (SE2) was used to charac- of the North China Platform (Wang et al., 1985). Various zircon terize topographic features, and an AsB detector was used to re- U-Pb ages have been reported from the Mesoproterozoic succes- veal compositional difference (backscattered electron, BSE, image). sion in North China (Fig. 1D; Li et al., 2010, 2014; Su et al., 2010; Samples were coated with 6-nm-thick platinum for electric con- Tian et al., 2015; Zhang et al., 2015). Based on the existing radio- duction before analysis. A Gatan ChromaCL2 cathodoluminescence metric ages and stratigraphic relationships, the base and top of the (CL) detector connected to the FESEM was used to obtain CL im- Gaoyuzhuang Formation are approximately assigned at ca. 1.60 Ga ages under 8 kV accelerating voltage with ∼30 min scanning time and ca. 1.54 Ga, respectively (Gao et al., 2009, 2010; Li et al., 2010). for each image. Element concentrations of micron-sized spots were The Gaoyuzhuang Formation is dominated by carbonates and quantitatively analyzed by an Oxford X-act energy dispersive X- can be subdivided into four members in the Yanqing area (Figs. 1D ray spectrometer (EDS) connected to the FESEM, operated at 20 and 2). Member I consists of cross-bedded sandstones in the low- kV with a working distance of ∼15 mm and a beam diameter of ermost part and stromatolitic dolostones in the upper part, which ∼2μm. Minerals as well as synthetic phases (MINM25-53) were M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 3

Fig. 1. Geological background of the study area. (A) Major tectonic subdivisions of China. The box shows the area illustrated in panel B. (B) Generalized Mesoproterozoic paleogeographic map of the central North China Platform (modified after Wang et al., 1985). (C) Simplified geological map of the study area, showing locality of the studied section (modified after the 1:200,000 Geological Map of China, The China Geological Survey, 2013). (D) Stratigraphic columns of the Jixian Group and Gaoyuzhuang Formation in the Yanqing area, northern suburb of Beijing. Samples were collected from the upper part of Member II and Member III of the Gaoyuzhuang Formation (Li et al., 2010; Tian et al., 2015)that covers the intervals correlated to the horizons yielding large eukaryotic fossils (Zhu et al., 2016), Grypania (Niu, 1998;Sun et al., 2006)and Chuaria (Sun et al., 2006). The ages in panel D are adopted from Li et al. (2010, 2014), Su et al. (2010), Tian et al. (2015), Zhang et al. (2015)and from those summarized in Zhu et al. (2016)and Tang et al. (2017a). (For interpretation of the colors in the figure(s), the reader is referred to the web version of this article.) 4 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

Fig. 2. (A) Stratigraphic column and sedimentary facies of the Gaoyuzhuang (GYZ) Formation in the Gan’gou section, Yanqing. (B) Medium-bedded muddy dolostone with mud-cracks and ripple marks on bedding surface, indicative of shallow subtidal to intertidal facies; upper Member II of the GYZ Formation. (C) Medium- to thinly-bedded muddy dolostone, suggestive of deep subtidal to outer shelf facies around the storm wave base; Member III of the GYZ Formation. (D) Thinly-bedded, dark-gray muddy dolostone without wave-agitated structures, indicative of deep subtidal facies below fair-weather wave base; Member III of the GYZ Formation. (E) Centimeter- to decimeter- sized carbonate concretions in calcareous mudstone, suggestive of outer shelf facies close to the storm wave base; Member-III of the GYZ Formation. (F) Thrombolites with millimeter-scale mesoclots, indicative of shallow subtidal facies; Member III of the GYZ Formation. (G) Microbially-laminated muddy dolostones with chert bands, indicative of shallow subtidal to intertidal facies; Member III of the GYZ Formation. (H) Schematic diagram showing facies subdivisions used in panels A–G. M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 5 used as reference standards. Duplicate analyses of individual points tage isotope ratio mass spectrometer (IRMS). Analytical uncertainty 13 showed analytical error less than 2%. was less than 0.2h (1σ ) for δ Corg based on replicate analyses 13 For phosphorus (P), aluminum (Al) and strontium (Sr) content of two international standards (USGS40, δ Corg =−26.39h; IVA- 13 analyses, ∼5 g of sample powders were directly measured using Urea, δ Corg =−37.32h). a handheld energy dispersive XRF spectrometer (HHXRF) model The total organic carbon (TOC) contents were analyzed at CUGB. Xsort with a Rh anode from Spectro, following the method de- About 10 g sample powders were weighed, decarbonated with 10% scribed in Tang et al. (2017b). The analytical uncertainty moni- HCl, rinsed by deionized water and dried. About 200 mg decar- tored by international reference material BCR-2 (Basalt) and JDo-1 bonated residues were weighed and wrapped in tin capsules and (dolostone) was ≤7% (Table S1). For calcium (Ca) and magnesium analyzed using an Elementer Macro Cube element analyzer. The (Mg) analyses, ∼5 g of sample powders were rinsed 4 times with uncertainty monitored by replicate analyses of an internal standard 18.25 M Milli-Q (MQ) water to remove clay minerals (Tang et was ≤0.1%. al., 2017b) and any soluble salts. After drying, the samples were grounded again into smaller and more homogenized powders in 4. Results an agate mortar. Finally, ∼5 mg rinsed dry powders were weighted and dissolved with 3% HNO3 and then diluted to 1:50,000 with All 234 samples were petrographically examined and 12 rep- 2% HNO3 before analyses. Concentrations were measured using a resentative samples were selected for CL and EDS analyses. Pet- PerkinElmer NexION 300Q Inductively Coupled Plasma Mass Spec- rographic observations show that calcite and dolomite grains are trometry (ICP-MS) at the National Research Center for Geoanalysis, mainly ∼20 μm in size and rarely larger than 50 μm (e.g., Figs. 3 Beijing. A certified reference material JDo-1 (dolostone) was mea- and 4). CL image shows that most calcite and dolomite grains are sured after every nine samples and the analytical uncertainties non-luminescent, with some dolomite grains in the middle part monitored by JDo-1 (n = 16) were <3% for Mg and <2% for Ca of the studied section displaying a non-luminescent core and dull (Table S2). luminescent rim (Fig. 3). This core-rim structure can also be iden- For iodine analyses, ∼5 mg of MQ water rinsed, dry powders tified in BSE image, with dark cores and relatively light outer rims were weighed. Nitric acid (3%) was added for dissolution and then (Fig. 4A). Quantitative EDS analyses show that the core is of low centrifuged to obtain supernatant. To stabilize iodine, 3% tertiary Mn and Fe contents while the light rim is slightly enriched in amine solution was added to the supernatant, and then diluted Mn and Fe (Fig. 4B; Table S5). The calcite has low Mn and Fe to 0.5% with MQ water (Hardisty et al., 2017;Lu et al., 2010). contents (Fig. 4B; Table S5). In addition, authigenic apatite grains The iodine content was measured within 48 hours to avoid any (commonly <10 μm in diameter) were identified in Member III iodine loss (Lu et al., 2010), using a Sector Field Inductively Cou- samples, with euhedral to anhedral morphology (Fig. 4C–H). pled Plasma Mass Spectrometry (SF-ICP-MS; Element XR, Thermo The most prominent feature of the study interval is the pos- Fisher Scientific, Germany) at the State Key Laboratory of Geo- itive shift in I/(Ca+Mg) ratios from Member II to Member III of logical Processes and Mineral Resources, China University of Geo- the Gaoyuzhuang Formation (Fig. 5; Table S6). The variation of science (Wuhan) (CUGW). The sensitivity of iodine was tuned to I/(Ca+Mg) ratios can be divided into four stages (Fig. 5). Stage ∼110 kcps for a 1 ppb standard in the SF-ICP-MS. The rinse solu- I (0–60 m) has I/(Ca+Mg) values between 0.0 μmol/mol and tion used for each individual analysis contains 0.5% HNO3, 0.5% ter- 0.5 μmol/mol. The I/(Ca+Mg) ratios increase from ∼0.5 μmol/mol tiary amine, and 50 μg/g Ca, and the typical rinse time is ∼1 min. to ∼2.0 μmol/mol in stage II (60–147.9 m). In stage III (147.9–220 Analytical uncertainties for 127I monitored by the internal standard m), I/(Ca+Mg) ratios reach the highest value of 3.8 μmol/mol, with GSR 12 and duplicate samples are ≤6% (1σ ) (Table S3). The long 30% of data points (9 of 30) higher than 2.6 μmol/mol. Almost term accuracy is checked by repeated analyses of the reference ma- all the I/(Ca+Mg) ratios return back to ≤0.5 μmol/mol in stage terial GSR 12 (Table S3). The detection limit of I/(Ca+Mg) is on IV (220–274.5 m). the order of 0.1 μmol/mol. Considering the significance of samples Estimates from previously published data suggest that more with high iodine concentrations, we re-analyzed these samples us- than 95% of the Proterozoic samples (n = 466) have I/(Ca+Mg) ra- ing MC-ICP-MS (Neptune Plus, Thermo Fisher Scientific, Germany) tios of <0.5 μmol/mol excluding the samples from intervals with at the National Research Center of Geoanalysis, Beijing, in order an oxygen rise (Fig. 6; Hardisty et al., 2017;Lu et al., 2017). Thus, to obtain more precise results. The sensitivity of iodine was tuned the value of 0.5 μmol/mol has been taken as the baseline for to ∼1,500 kcps for a 1 ppb standard in the MC-ICP-MS, and the I/(Ca+Mg) ratios in Precambrian carbonates (Lu et al., 2017). The analytical uncertainties of 127I monitored by the internal standard I/(Ca+Mg) ratios in stage III of the study interval (Fig. 5) are higher GSR 12 and duplicate samples are ≤7% (1σ ; Table S3). The repro- than the maximum values reported from the mid-Proterozoic sam- ducibility of most I contents and I/(Ca+Mg) ratios measured by the ples up to date, but similar to those of the diagenetically altered two ICP-MS setups is better than 90% (Table S4). carbonates found in sediments from the Clino core in the Ba- 13 Carbonate carbon isotopes (δ Ccarb) were analyzed at the LVIS hamas (Fig. 6; Hardisty et al., 2017). They are also higher than Lab of the University of Nevada Las Vegas. About 50–200 μg of those reported from the carbonates across the Great Oxidation carbonate powders were reacted with orthophosphoric acid for 10 Event (GOE) at ca. 2.3–2.4 Ga (∼2 μmol/mol; Hardisty et al., 2014), ◦ min at 70 C in a Kiel IV device connected to a Finnigan Delta Plus but are markedly lower than the highest I/(Ca+Mg) values across dual-inlet mass spectrometer. The precision monitored by NBS-19 the Bitter Springs δ13C anomaly (∼8 μmol/mol; 810–800 Ma; Lu 13 18 and an internal standard (USC-1; δ Ccarb = 2.09h; δ Ocarb = et al., 2017;Wörndle et al., 2019) and the Ediacaran Shuram −2.08h) is better than 0.08h for both C and O isotopes. Organic δ13Cexcursion (∼8 μmol/mol; ca. 580 Ma; Hardisty et al., 2017; 13 carbon isotopes (δ Corg) were analyzed at the State Key Labora- Wei et al., 2019). tory of Biogeology and Environmental Geology, CUGW. About 2 g The positive shift in I/(Ca+Mg) is accompanied by an increase of sample powders were decarbonated using 10% HCl at room tem- of phosphorus (P) contents and P/Al ratios (Fig. 5; Table S6). Dur- perature for 48 hours. The carbonate-free residue was then rinsed ing stage I, P concentrations were stable and close to 0.05 wt%, with deionized water repeatedly until the pH reached nearly neu- comparable to the mean value of pre-Cryogenian shales (0.051 ± ◦ tral, centrifuged and dried at 45 C. Dried samples were powdered, 0.003 wt%; Reinhard et al., 2017). During stage II, P contents were weighed (5–20 mg), and wrapped in tin capsules and combusted at highly variable (0.00–0.13 wt%), with peak values at the top part ◦ 960 C in an Elemental Analyzer (Thermo Fisher). The CO2 released that are comparable to the mean value of post-Tonian shale sam- 13 from organic matter was analyzed for δ Corg by a Delta V Advan- ples (0.209 ± 0.023 wt%; Reinhard et al., 2017). The P contents 6 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

Fig. 3. Examples of Scanning Electron Microscope (SEM) and Cathodoluminescence (CL) images showing the textural and diagenetic features of carbonates from the study section. (A) Secondary electron (SE) image of a dolomite (Dol) from stage I in Fig. 5. (B) CL image of the same area in panel A, showing non- to dull (orange red) luminescence. (C) SE image of a dolomitic limestone showing calcite (Cal) and dolomite (Dol, arrows) from stage II in Fig. 5. (D) CL image of the same area in panel C, showing that calcite has non-luminescence and dolomite has the non-luminescent core and dull (orange red) luminescent rim (arrows). (E) SE image showing calcite (Cal) and dolomite (Dol, arrows) of a dolomitic limestone from stage III in Fig. 5. (F) CL image of the same area in panel E, showing non-luminescent calcite, and the non-luminescent core and dull (red) luminescent rim (arrows) of dolomite. (G) SE image showing calcite (Cal) and dolomite (Dol, arrows) of a dolomitic limestone from stage IV in Fig. 5. (H) CL image of the same area as in panel G, showing mainly non-luminescent calcite and dolomite. The magnification of all the panels are the same as in panel A. M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 7

Fig. 4. SEM image and EDS analysis of the Gaoyuzhuang carbonates. (A) Backscattered electron (BSE) image showing the core-rim structure of dolomite grains (arrows). (B) Cross plot of the Mn and Fe contents of calcite and the core and rim of dolomite (Table S5). Both calcite and the core of dolomite have low Mn and Fe contents, but the rim of dolomite has relatively high Mn and Fe contents. (C) SE image showing an euhedral apatite. (D) SE image showing subhedral to euhedral apatite aggregates. (E) Close view of the apatite aggregates in panel D. (F) BSE image showing anhedral apatite. (G) BSE image showing globular apatite aggregates. (H) EDS spectrum of the apatite in panel G. All the apatite grains were from Member III of the Gaoyuzhuang Formation. 8 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

13 13 Fig. 5. Profiles of I/(Ca+Mg), P, P/Al, δ Ccarb and δ Corg of Member II and III of the Gaoyuzhuang Formation at Gan’gou, Yanqing County, north of Beijing. The smoothed thick lines represent the LOESS curves. In the I/(Ca+Mg) profile, the vertical red dashed line at 0.5 μmol/mol marks the I/(Ca+Mg) baseline—the maximum [O2] level of 10 μM that could be produced by local primary production, and the red dashed line at 2.6 μmol/mol represents the estimated [O2] of >20–70 μM. In the profile P and P/Al, the vertical red dashed line at 0.05 wt% marks the mean value of P concentrations in pre-Cryogenian shales (0.051 ± 0.003 wt%; Reinhard et al., 2017). Positive shift in 13 13 I/(Ca+Mg) coincides with the increase in P and P/Al, and is accompanied with a negative shift in δ Ccarb and δ Corg.

13 13 range from 0.00 to 0.09 wt% during stage III and fall back to near overall both δ Ccarb and δ Corg reach their minimum values at zero at stage IV (Fig. 5). Consistent with the high P contents, au- the interval with highest I/(Ca+Mg) ratios. thigenic apatite grains were identified in the carbonate samples of stage II and III (Fig. 4). The presence of authigenic apatite (Fig. 4) 5. Discussion and co-varying P/Al and P content (Fig. 5) suggest that the pos- itive shift in P content was not caused by siliciclastic input. For 5.1. Primary vs. diagenetic signals samples with TOC contents >0.2%, the P/TOC ratios also show an + increase from stage I to stage III and a decrease in stage IV (Table Carbonate I/(Ca Mg) ratios are susceptible to diagenetic alter- S6), suggesting that the P change was not caused by TOC variations ation (Hardisty et al., 2017;Lu et al., 2010;Zhou et al., 2015; Wörndle et al., 2019). During diagenesis, carbonate-associated io- in these carbonates. However, some low TOC samples (TOC <0.2%), − − date (IO ) is reduced to iodide (I ) and is excluded from carbonate particularly those from stage I, have higher P/TOC ratios. Consider- 3 + ing the 0.1% uncertainty related to TOC measurement, these high lattices, thus lowering the I/(Ca Mg) ratios of carbonates (Hardisty et al., 2017;Lu et al., 2010). Since iodide cannot enter the lat- P/TOC ratios may have been exaggerated by the low TOC rather tice of carbonate minerals, likely due to its large ion radius (Lu et than high P contents (Table S6). al., 2010), most diagenetic processes would decrease rather than Both δ13C and δ13C show a negative excursion (Table S6) carb org increase the I/(Ca+Mg) ratios (Hardisty et al., 2017). In this re- that accompanies the positive shift in I/(Ca+Mg) ratios (Fig. 5). The gard, the prominent increase in I/(Ca+Mg) from ∼0.5 μmol/mol δ13C values range from 0% to −2h in stages I and II, and reach carb to >2.6 μmol/mol in stage II and III of the Gaoyuzhuang For- − h 13 the minimum of 3.5 at stage III (Fig. 5). This negative δ Ccarb mation (Fig. 5) is unlikely an artifact of diagenesis. In fact, the excursion has also been reported from the sections in the Ming I/(Ca+Mg) values may have been initially higher; i.e., the observed Tombs (Li et al., 2003), Jixian (Zhang et al., 2018), and Pingquan peak should be regarded as a minimum estimate of local seawater (Guo et al., 2013)of North China (Fig. 7), suggesting that it is iodate levels. 13 13 at least a regionally consistent δ Cexcursion. The δ Corg val- Liberation of iodine from organic matter during chemical anal- ues show some variations between −29h and −32h in stage I, ysis may artificially increase the I/(Ca+Mg) ratio, but iodine in and a decline to the minimum values around −34h in stage III organic matter is tightly bonded and hard to be liberated (Zhou 13 (Fig. 5). There are some variations between the negative δ Ccarb et al., 2015, 2017). During the sectioning and chemical analyses, 13 and δ Corg excursions, and the increase in I/(Ca+Mg) ratios oc- we have avoided samples that have dark color (potentially high 13 curs stratigraphically ∼10 m below the decrease in δ Ccarb, but TOC) and used diluted acid (3% nitric acid; Lu et al., 2010) to min- M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 9

Fig. 6. Secular variations in I/(Ca+Mg) through time (modified from Hardisty et al., 2017; Lu et al., 2017, 2018). Vertical blue bars mark the intervals where the I/(Ca+Mg) data are consistent with possible oxygenation events (Gilleaudeau et al., 2016;Kendall et al., 2009;Planavsky et al., 2014; Zhang et al., 2016)relative to the long term atmospheric p[O2] curve (Lyons et al., 2014;Planavsky et al., 2014;Sperling et al., 2015)and biological production of O2 (Cox et al., 2018). The vertical orange bars mark the multi-cellularization of eukaryotes in the Mesoproterozoic (e.g., Zhu et al., 2016) and the diversification of eukaryotes in the Neoproterozoic (Mills et al., 2014), respectively. The grey dashed line at 0.5 μmol/mol marks the Precambrian I/(Ca+Mg) baseline and the grey dashed line at 2.6 μmol/mol represents the threshold of [O2] >20–70 μM. imize the iodine from noncarbonate phases (cf. Zhou et al., 2017; zoic samples (Fig. 8F). Most high I/(Ca+Mg) values are from sam- Wörndle et al., 2019). In addition, sample powder was rinsed 4 ples that have relatively high δ18O and Sr contents (Fig. 8G and times to remove loosely absorbed iodine on the surface of min- H), suggesting that meteoric diagenesis may not be a major con- erals. The lack of correlation between I/(Ca+Mg) and (CaO+MgO) trolling factor of the I/(Ca+Mg) ratios (cf. Wörndle et al., 2019). (Fig. 8A), I/(Ca+Mg) and TOC (Fig. 8B), I/(Ca+Mg) and Al (Fig. 8C), The CL observation shows that calcite and dolomite display non- but a strong correlation (R2 = 0.97) between I/(Ca+Mg) and I to dull luminescence (Fig. 3) indicative of low Mn and Fe con- (Fig. 8D) suggest that the I/(Ca+Mg) is controlled by the iodine tents that also suggest limited influence from meteoric diagen- content in carbonates, rather than the carbonate and TOC contents esis. Some dolomite grains show core-rim structure in both CL of the samples. Therefore, the iodine from noncarbonate phases in- and BSE images. The core is non-luminescent (CL) or dark (BSE) cluding organic matter may not be a significant contributor to the with low to undetectable Mn and Fe contents, while the rim is positive shift in I/(Ca+Mg) (Fig. 5). dull (CL) and light (BSE) with relatively high Mn and Fe con- The highest I/(Ca+Mg) values are present in partially dolomi- tents (Figs. 3 and 4). These features suggest that the rims of tized samples (Fig. 8E) and their distribution in the cross plot dolomite grains were likely formed in the Mn reduction zone, of I/(Ca+Mg) vs. Mg/Ca is similar to that of the other Protero- while the nuclei were possibly primary precipitates or formed in 10 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

13 Fig. 7. Correlation of the negative δ Ccarb excursion and fossil-bearing interval in Member III of the Gaoyuzhuang Formation of the North China Platform at Gan’gou, Yanqing, northern suburb of Beijing (this study), the Ming Tombs, ∼35 km north of Beijing (Li et al., 2003), Jixian, Tianjin, ∼100 km east to Beijing (Zhang et al., 2018), and Pingquan, Hebei Province (Guo et al., 2013). In addition, macroscopic fossils are found in the Qianxi and Kuancheng sections, Hebei Province (Zhu et al., 2016). The interval with Ce anomaly data from the Jixian section (Zhang et al., 2018)is also marked. the nitrate-reduction zone (Canfield and Thamdrup, 2009;Liu et netic overprint from the redox-controlled water-column signal in al., 2019). Since nitrate and Mn reduction zones are commonly those samples; however, petrographic and CL observations did not very shallow and the reduction potential of Mn-oxide, iodate, and show significant mineralogical and textural differences between nitrate is very close to each other (Canfield and Thamdrup, 2009; the samples that have low (stage I and IV) and high (stage II Lu et al., 2010), partial dolomitization within the Mn and nitrate and III) I/(Ca+Mg) values (Fig. 5). Thus, we consider that the low reduction zones must have happened during early diagenesis near I/(Ca+Mg) values of stage I and IV record more reduced water col- the seawater/sediment contact where porewater was exchangeable umn conditions. with the overlying seawater. During early diagenesis, seawater or − seawater-derived fluids may progressively transfer IO (and other 3 5.2. Carbonate I/(Ca+Mg) as a semi-quantitative redox proxy ions and cations) into authigenic carbonates precipitated from porewater (e.g., Ahm et al., 2018; Higgins et al., 2018). However, − Iodine-to-calcium-magnesium [I/(Ca+Mg)] ratios of carbonate because IO3 is the only iodine species that can be incorporated − rocks represent one of the few geochemical proxies that track into carbonate minerals (Lu et al., 2010), the resulting IO3 con- tent and I/(Ca+Mg) ratio would not exceed that of the overlying the redox condition of shallow oceans (e.g., Hardisty et al., 2017; seawater. In the samples we have analyzed, large (>50–100 μm) Lu et al., 2010, 2016). Dissolved iodine in seawater has two ma- jor thermodynamically stable forms: the oxidized species iodate euhedral dolomites were rarely observed, suggesting that subse- − − quent burial diagenesis had limited effects on mineral textures and (IO3 ) and reduced species iodide (I ). Iodate is the dominant potentially, chemical compositions. form in oxic waters and is quantitatively reduced to iodide to- The low but non-zero (mostly ≤0.5) I/(Ca+Mg) values in stage wards the core of the oxygen minimum zone (OMZ) or in anoxic + waters (Emerson et al., 1979;Lu et al., 2010;Luther and Camp- I and IV (Fig. 5) fall into the I/(Ca Mg) range of diagenetically al- − tered samples (Hardisty et al., 2017), raising the possibility that bell, 1991). Since IO3 is the only iodine species that can incor- diagenesis may have significantly lowered the I/(Ca+Mg) ratios in porate into the lattice of carbonate minerals, carbonates precipi- these intervals. These values, however, are also within the range tated from oxic waters would have high I/(Ca+Mg) ratios, while of I/(Ca+Mg) ratios obtained from modern and ancient carbon- those precipitated closer to the OMZ or anoxic waters record lower ates that were deposited in suboxic to anoxic environments (Glock I/(Ca+Mg) ratios (Lu et al., 2010, 2016). Diagenetic alteration may et al., 2014; Hardisty et al., 2014, 2017; Lu et al., 2010, 2016; lower the I/(Ca+Mg) of primary carbonates, but it would not in- Zhou et al., 2015). Particularly, they are within the range of crease the I/(Ca+Mg) in carbonate rocks (Hardisty et al., 2017; I/(Ca+Mg) values of Proterozoic samples from different deposi- Wörndle et al., 2019). Our petrographic observations suggest that tional environments (Fig. 6; Hardisty et al., 2017). Without addi- dolomitization of the Gaoyuzhuang Formation carbonates occurred tional analyses such as Ca and Mg isotopes (e.g., Ahm et al., 2018; during early diagenesis and the I/(Ca+Mg) ratios may record the − Higgins et al., 2018), it is difficult to separate the potential diage- minimum estimate of water column [IO3 ] (and free O2) avail- M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 11

Fig. 8. Cross plots of the Gaoyuzhuang geochemical data. (A) I/(Ca+Mg) vs. (CaO+MgO), (B) I/(Ca+Mg) vs. TOC, (C) I/(Ca+Mg) vs. Al, (D) I/(Ca+Mg) vs. I, (E) I/(Ca+Mg) vs. Mg/Ca of the Gaoyuzhuang samples. The positive correlation between I/(Ca+Mg) and I indicates that the high I/(Ca+Mg) ratios relate to high iodine concentrations in carbonates. (F) Comparison of the I/(Ca+Mg) vs. Mg/Ca of the Gaoyuzhuang samples with those of the modern and ancient carbonates (Hardisty et al., 2017;Lu et al., 2017). (G) I/(Ca+Mg) vs. δ18Oof the Gaoyuzhuang samples. (H) I/(Ca+Mg) vs. Sr of the Gaoyuzhuang samples. ability in the depositional environment (Feng and Redfern, 2018; al., 2014, 2017). Since diagenetic alternation of carbonates com- Hardisty et al., 2017;Lu et al., 2010). monly proceeds in suboxic to anoxic conditions, I/(Ca+Mg) values Previous studies suggested that a minimum of 1–3 μM [O2] of carbonates should be lower than that of the primary carbon- − + is required for marine IO3 accumulation and for the presence of ate sediments (Hardisty et al., 2017). In rare cases, the I/(Ca Mg) carbonate-bound iodine (Hardisty et al., 2014, 2017). This require- values of carbonates could be higher than that of the primary pre- ment is supported by observations in the OMZs along the eastern cipitates if the diagenetic fluids were highly oxic. However, this is coast of the north Pacific (e.g., Rue et al., 1997), the Arabian Sea unlikely for the Gaoyuzhuang Formation because (1) none of the (e.g., Farrenkopf and Luther, 2002; Farrenkopf et al., 1997), and adjacent Mesoproterozoic stratigraphic units produced higher (e.g., in other modern anoxic basins (Luther and Campbell, 1991). In >4 μmol/mol) I/(Ca+Mg) ratios (Fig. 6; Hardisty et al., 2017) and depositional environments where the OMZ is present, oxygen con- (2) field, petrographic, and mineral observations exclude the pos- centrations vary from ∼225 μM near the ocean surface to 1–3 sibility that the Gaoyuzhuang Member III served as a conduit of − μM in the center of the OMZ, with IO3 concentrations decreas- highly oxic, Phanerozoic diagenetic fluids. ing from >0.25 μM to ∼0.01 μM (Rue et al., 1997). Consequently, In modern oceans, due to biotic absorption of iodine and tem- I/(Ca+Mg) > 0.1 μmol/mol was suggested as an indicator for porospatial redox variations (e.g., the presence/absence of OMZ), ≥ − water-column O2 concentration of 1–3 μM (Table 1; Hardisty et seawater IO3 and O2 concentrations commonly do not show a 12 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

Table 1 Semi-quantitative estimation of surface ocean O2 using I/(Ca+Mg) ratios of carbon- ates. + − I/(Ca Mg) [IO3 ] [O2] References (μmol/mol) (μM) (μM) ∼0.0 <0.01 <1–3 Hardisty et al., 2014, 2017 0.0–0.5 ≤0.05 ≤10 cf. Olson et al., 2013; Reinhard et al., 2016; Lu et al., 2017 0.5–2.6 ≤0.25 ≤20–70 Lu et al., 2016 >2.6 >0.25 >20–70 Lu et al., 2016 perfect linear relationship (e.g., Lu et al., 2016; Zhou et al., 2014, − 2015). Lu et al. (2016) compiled the IO3 , I/Ca, and O2 concentra- tion data from modern anoxic basins and ocean water columns with the presence of an OMZ. The results show that the I/Ca values obtained from the modern and late Holocene planktonic ∼ − foraminifera have I/Ca > 2.5 μmol/mol corresponding to IO3 concentrations of >0.25 μM and O2 concentrations >20–70 μM in the water column (Table 1; Lu et al., 2016). The incorporation of iodate into biogenic and abiogenic carbonates could be slightly dif- − ferent: IO3 may be preferentially incorporated into three naturally- occurring polymorphs of calcium carbonate in the order of va- terite > calcite > aragonite (Feng and Redfern, 2018). Considering this effect, Hardisty et al. (2017) adjusted the I/(Ca+Mg) ratio of >2.6 μmol/mol as an indicator of water-column O2 concentrations of >20–70 μM. The oxygen concentrations corresponding to the I/(Ca+Mg) values of 0.0–2.6 μmol/mol are less well constrained. However, existing data from anoxic basins and from the ocean wa- ter column with the presence of an OMZ (e.g., Glock et al., 2014; Lu et al., 2016; Zhou et al., 2014, 2015) demonstrated that when + − I/(Ca Mg) <0.5 μmol/mol, the corresponding [IO3 ] levels are <0.05 μM and the O2 concentrations are mostly <10 μM (Table 1). The Precambrian iodine reservoir might be slightly larger than or similar to that of the Phanerozoic due to less efficient up- take and burial of iodine by primary producers, particularly al- gae (Hardisty et al., 2017). However, because I/(Ca+Mg) tracks − − + IO3 rather than I , the I/(Ca Mg) ratio was mainly controlled by water-column redox conditions, not the iodine reservoir size (Hardisty et al., 2017). Therefore, the relationship between [O2] and carbonate I/(Ca+Mg) ratio may have been similar in Precam- brian and modern surface oceans. If this reasoning is correct, the I/(Ca+Mg) ratios from the modern environments (Table 1) may be used to semi-quantitatively estimate the temporal O2 changes across the study interval (Fig. 5).

5.3. A pulse of oxygen increase at ca. 1.57–1.56 Ga

The atmospheric oxygen level during the mid-Proterozoic has been debated. Some studies proposed that the mid-Proterozoic oxygen concentration was <0.1–1% PAL (Planavsky et al., 2014; Cole et al., 2016), while others argued that the O2 concentra- Fig. 9. Schematic interpretation for the pulse of oxygen increase in the upper tion was much higher (>1% PAL or >4% PAL; Gilleaudeau et al., Gaoyuzhuang Formation (referring to the temporal change of data in Fig. 5). In stage 2016; Zhang et al., 2016, 2017; Canfield et al., 2018). To date, mid- I, the increase of primary productivity and organic carbon burial led oxygen increase 13 and a relatively heavy δ C. In stage II and III, accumulation of dissolved O2 resulted Proterozoic intervals marked with high atmospheric oxygen are − + in higher IO3 concentrations in the surface ocean and higher carbonate I/(Ca Mg) only identified at 1.4 Ga (e.g., Zhang et al., 2016, 2017; Hardisty ratios. Oxidation of DOC led to the negative δ13C excursion and P enrichment. In ∼ et al., 2017) and 1.3–0.9 Ga (e.g., Gilleaudeau et al., 2016; stage IV, oxidation of DOC consumed oxygen and returned back to low O2 level. Canfield et al., 2018). There is no evidence for persistently high O2 concentrations during the period of 1.8–1.4 Ga. The increase of I/(Ca+Mg) ratios from <0.5 μmol/mol to peak values of ≥2.6 μmol/mol in the Gaoyuzhuang Formation (Fig. 5) values are from the interval with relatively greater depositional is unlikely resulted from the shoaling of the carbonate platform water depth (Figs. 2 and 5). There is no temporal relationship be- which may have pushed the oxycline to a greater water depth. tween I/(Ca+Mg) and facies changes. Therefore, we interpret that Most carbonates of the Gaoyuzhuang Formation in the Yanqing the positive I/(Ca+Mg) anomaly in the Gaoyuzhuang Formation area were deposited from shallow-water environments above the may record a pulse of oxygen increase in the surface ocean and storm wave base (Tang et al., 2016) and the highest I/(Ca+Mg) atmosphere (Fig. 9). M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 13

Taking the semi-quantitative correlation between I/(Ca+Mg) (e.g., Bristow and Kennedy, 2008). A simple mass balance calcula- 13 and minimum O2 levels obtained from seawaters adjacent to OMZs tion indicates that a −3.5h δ Cexcursion formed through oxi- and in anoxic basins as a reference (Table 1), the I/(Ca+Mg) val- dation of oceanic DOC (δ13C ≈−25h) would require ∼ 5.6 × 1017 ues of <0.5 μmol/mol (but non-zero) in stage I (Fig. 5) would moles of O2 (cf. Dickens et al., 1995), which amounts to ∼1.9% 19 imply water column O2 concentrations between 1–3 μM and 10 PAL (∼ 3.9 × 10 moles or 21% atmospheric O2) or 2.5 times of 17 μM, which are lower than the maximum O2 concentration (<10 the total dissolved O2 in the modern ocean (∼ 2.3 × 10 moles of 13 μM) that can be produced by local oxygenic primary produc- O2). Considering that the duration of the δ C anomaly might be tion in the surface ocean (e.g., Kasting, 1991;Olson et al., 2013; longer than the carbon residence time (105 years), the amount of Reinhard et al., 2016). This estimate is consistent with many other O2 (oxidants) requirement would be higher than the amount sug- studies that show generally low O2 levels in the Mesoprotero- gested by the mass balance calculation (cf. Bristow and Kennedy, zoic surface ocean and atmosphere (e.g., Planavsky et al., 2014; 2008). Of course, the Mesoproterozoic dissolved inorganic carbon Reinhard et al., 2016). The I/(Ca+Mg) values between 0.5 μmol/mol (DIC) pool could also be different from that of the modern ocean and 2.6 μmol/mol in stage II (Fig. 5) may record seawater O2 (Rothman et al., 2003) and the increase of P may facilitate pri- concentrations between 10 μM and 20–70 μM, which is higher mary production and oxygen increase, which complicates the O2 than the maximum O concentration attainable through local oxy- 2 estimation. Nonetheless, the consumption of O2 (oxidants) by oxi- genic primary production (e.g., Reinhard et al., 2016). Therefore, dation or remineralization of DOC remains the simplest interpreta- + the increase of I/(Ca Mg) from 0.5 μmol/mol to 2.6 μmol/mol may tion for the “short-lived” pulse of oxygen increase implied by the record the initial increase of atmospheric oxygen at this time. The I/(Ca+Mg) ratios from the Gaoyuzhuang Formation (Figs. 5 and 9). + peak I/(Ca Mg) values of >2.6 μmol/mol (up to 3.4 μmol/mol) The increase of oxygen during ca. 1.57–1.56 Ga is also sup- ≥ in stage III likely suggest seawater O2 concentrations 20–70 μM ported by the negative shift in cerium (Ce) anomaly from the (Table 1). During this stage, even if oxygenic primary production Jixian Section in North China (Zhang et al., 2018). To date, how- resulted in a 10 μM O2 concentration in the surface ocean (e.g., ever, there is no documentation of this event from other con- Kasting, 1991;Olson et al., 2013; Reinhard et al., 2016), it would tinents globally, possibly due to the lack of precise ages and ≥ still require a significant increase ( 10–60 μM) in surface ocean appropriate stratigraphic record that warrants future investiga- O2 contributed from the atmosphere. Taking the average O2 con- tion. In contrast, the rise of oxygen at ca. 1.4 Ga has been centration of 250 μM as a reference for the modern surface ocean documented from many sections in multiple continents includ- (Garcia et al., 2013), a ≥10 μM increase in surface ocean O would 2 ing North China (Cox et al., 2016; Hardisty et al., 2017; Zhang imply that the atmospheric oxygen concentration was ≥4% PAL at et al., 2016, 2017), North Australia (Mukherjee and Large, 2016; the time. There is an apparent decrease of I/(Ca+Mg) values in Yang et al., 2017) and West Siberia (Sperling et al., 2014). There stage IV (Fig. 5). Similar to those seen in stage I, most samples is uncertainty on whether the increase of oxygen started at ca. from stage IV have I/(Ca+Mg) values of ≤0.5 μmol/mol, suggest- 1.57 Ga and continued through ca. 1.4 Ga, but the lack of evidence ing a surface ocean O level of ≤10 μM. If these I/(Ca+Mg) values 2 for persistent oxidation between ca. 1.57 Ga and ca. 1.4 Ga sug- were not significantly lowered by diagenetic alteration, it implies gests that they represent two distinct episodes of Mesoproterozoic that the pulse of oxygen increase did not last long, perhaps on the oxygenation. The surface ocean and atmospheric O level (≥4% order of 10 million years from ca. 1577 ± 12 to 1560 ± 5 Ma, al- 2 PAL) estimated from the I/(Ca+Mg) ratios of the Gaoyuzhuang For- though the large uncertainty of available radiometric ages prevents mation is significantly higher than the 0.1%–1% PAL based on Cr a more precise estimation. isotopes (Cole et al., 2016;Crowe et al., 2013; Planavsky et al., A pulse of oxygen increase is consistent with the coupled nega- 13 13 2014). This discrepancy can be reconciled by pulsed oxygenation tive δ Ccarb and δ Corg anomalies and the increase of P/Al ratios under the background of long-lasting low oxygen levels. Our data at the same stratigraphic interval (Fig. 5). Negative δ13C anoma- show that, after the peak values in stage III, I/(Ca+Mg) values fall lies could be a result of oxidation of dissolved organic carbon (DOC) reservoir in the ocean (e.g., Rothman et al., 2003) or other back to Proterozoic baseline values (Fig. 5). Similar trends were + forms of reduced carbon such as methane (e.g., Bjerrum and Can- also found in other Proterozoic intervals that have high I/(Ca Mg) field, 2011), terrestrial organic matter (e.g., Kaufman et al., 2007) values, including the interpreted oxidation events at ca. 1.4 Ga, 0.8 and petroleum (e.g., Kroeger and Funnell, 2012), authigenic car- Ga, and 0.58 Ga (Fig. 6; Hardisty et al., 2017;Lu et al., 2017; + bonate precipitation (e.g., Schrag et al., 2013; Higgins et al., 2018), Wörndle et al., 2019). The secular variations in I/(Ca Mg) ra- and/or low primary production (e.g., Kump, 1991), and/or diagene- tios (Fig. 6) and many other geochemical data seem to support sis (Swart and Eberli, 2005;Swart, 2008;Derry, 2010;Oehlert and pulsed oxygenation events in an overall anoxic low productiv- Swart, 2014). The negative δ13C anomaly is accompanied by a pos- ity mid-Proterozoic ocean (Reinhard et al., 2016; Crockford et al., itive shift in I/(Ca+Mg), which was considered as evidence against 2018, 2019; Ozaki et al., 2019). diagenetic alteration in reduced environments (e.g., Hardisty et al., An unresolved issue relates to the cause of oxygenation dur- 2017). The interval with minimum δ13Cvalues has higher TOC ing ca. 1.57–1.56 Ga and other Proterozoic intervals. Increase of contents (Table S6), excluding the possibility of a sudden decrease primary productivity and organic carbon burial is the most effi- or shutdown of primary productivity. Although other possibili- cient way for an oxygen increase in atmosphere and ocean (e.g., ties may also exist, the most parsimonious interpretation for this Berner and Canfield, 1989;Berner et al., 2007). Increase of pri- negative δ13C anomaly would be oxidation of the oceanic DOC mary productivity and organic carbon burial is commonly accom- 13 reservoir, which has been suggested to be much larger (10–100 panied by a positive δ Cexcursion. So far there is no prominent 13 times) than that of modern ocean (Rothman et al., 2003). Oxida- positive δ Ccarb excursion documented from the lower part of tion of organic matter releases phosphorous (e.g., März et al., 2008; the Gaoyuzhuang Formation prior to the interpreted oxygenation 13 Reinhard et al., 2017), which explains the increase of P content event, although an up to 5h positive shift in δ Corg is present be- and P/Al ratio across the δ13C anomaly. Although the magnitude of low this interval (Luo et al., 2014). Most of the existing δ13C anal- the δ13C anomaly (−3.5h) is smaller than that of the late Neo- yses have been concentrated at the middle-upper Gaoyuzhuang proterozoic δ13C excursions, it is comparable with or even larger Formation and the underlying isotope record has low stratigraphic than those of the Phanerozoic negative δ13C excursions. Oxida- resolution (e.g., Guo et al., 2013;Li et al., 2003;Luo et al., 2014; tion of organic matter consumes oxygen (and oxidants) and may Zhang et al., 2018). A more detailed isotope analysis for the in- significantly lower the marine and atmospheric O2 concentrations tervals below the interpreted oxidation events at ca. 1.57–1.56 Ga 14 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 and other Proterozoic intervals remains to be investigated in future of oceanic DOC. Oxidation of DOC consumed oxygen (and ox- studies. idants) and subsequently lowered the marine and atmospheric O2 levels to the background Mesoproterozoic oxygen concentra- 5.4. Implication for eukaryotic evolution tion of ≤0.1–1% PAL (Planavsky et al., 2014;Cole et al., 2016). Multiple episodes of oxygen increase may have happened dur- Eukaryotes need oxygen for respiration and their minimum ing the mid-Proterozoic, including those at ca. 1.85 Ga (Planavsky oxygen requirements have been estimated as >0.1% PAL for some et al., 2018a), ca. 1.57–1.56 Ga (Tang et al., 2016; Zhang et simple forms and higher for more complex species (e.g., Mills et al., 2018), ca. 1.4 Ga (Cox et al., 2016; Hardisty et al., 2017; al., 2014;Sperling et al., 2013). Based on the oxygen diffusion Mukherjee and Large, 2016;Sperling et al., 2014; Yang et al., 2017; model, the size of eukaryotes scales with the minimum oxygen Zhang et al., 2016), ca. 1.33–1.08 Ga (Canfield et al., 2018), and ca. 1.1 Ga (Gilleaudeau et al., 2016), and these oxidation events requirement. Particularly, the minimum O2 requirements for the Mesoproterozoic macrofossil Grypania and Chuaria were estimated may have been short-lived due to the consumption of oxygen through oxidation of DOC and other reductants (such as reduced as higher than 1% PAL (Runnegar, 1991). The minimum O2 re- quirements for sponges, which are one of the earliest metazoan iron in the ocean). Only when oceanic DOC and reduced iron in groups, are in the range of 0.5–4% PAL (Mills et al., 2014). The esti- the ocean were largely consumed and the redoxcline was pushed mated atmospheric oxygen levels of >4% PAL during ca. 1.57–1.56 down to the deeper ocean, stable oxygenated surface environments Ga are apparently sufficient to support the respiration of Grypa- could be maintained to support complex eukaryotic ecosystems. Temporally isolated oxidation events in an overall anoxic mid- nia, Chuaria, and perhaps many of the early animals. Coincidentally, Proterozoic ocean explain the increase of multicellular eukaryotes decimeter-scale multicellular eukaryotes (Zhu et al., 2016), Grypa- at ca. 1.57–1.56 Ga (Zhu et al., 2016) and ca. 1.4 Ga (Mukherjee et nia (Niu, 1998;Sun et al., 2006), and Chuaria (e.g., Sun et al., 2006) al., 2018), but there is no evidence for continuous diversification are present at the interval with the highest I/(Ca+Mg) values in of eukaryotes between the oxidation events. the Gaoyuzhuang Formation (Fig. 5). Therefore, it is reasonable to assume that the increase of oxygen provided a more hospitable Acknowledgements environment for the multi-cellularization of early eukaryotes. The pathway that oxygen influenced the evolution of eukary- Thanks are given to the editor and three anonymous review- otes is not well understood. Oxygen could directly influence the ers for their constructive suggestions and comments, which greatly evolution of eukaryotes by meeting their respiration needs (e.g., improved the paper. Thanks also go to Wenhao Zhang, Jinjian Wu, Planavsky et al., 2014) and/or indirectly influence the evolution of Xianghe Li, Yun Liu and Yang Li for their assistance in the field. eukaryotes through modulating the nutrient cycle (e.g., N and P; We are grateful to Hongmei Yang, Chongpeng Liu, Zhaochu Hu, Zhao et al., 2018). The bioavailability of N and P in the oceans Tao He, Yong Du, Chao Wei and Xiang Li for their helps in sample is controlled by the redox conditions. More oxic oceans could − pretreatments and analyses. The study was supported by the Na- maintain a stable bioavailable N (mainly NO ) reservoir (e.g., 3 tional Natural Science Foundation of China (No. 41672336) and by Koehler et al., 2017; Wang et al., 2018), deepen the iron redox the Fundamental Research Funds for the Central Universities (Nos. chemocline, and reduce the P loss through Fe-oxide precipitation 2652018005 and 2652017050). (e.g., Hemmingsson et al., 2018). During the pulse of oxygena- tion identified in the Gaoyuzhuang Formation, oxygen concentra- Appendix A. Supplementary material tion was likely higher than the minimum requirements of those Gaoyuzhuang eukaryotes, and the nutrient elements, such as N and Supplementary material related to this article can be found on- P, may have been sufficient due to the expansion of more oxic con- line at https://doi .org /10 .1016 /j .epsl .2019 .115797. ditions and deepened iron-redox chemocline (Fig. 9). Therefore, the evolution of eukaryotes could be accelerated during the pulse of References oxygen increase. There is no evidence, however, for continued evolution and di- Ahm, A.S.C., Bjerrum, C.J., Blättler, C.L., Swart, P.K., Higgins, J.A., 2018. Quantifying versification of eukaryotes after ca. 1.56 Ga, and the first appear- early marine diagenesis in shallow-water carbonate sediments. Geochim. Cos- ance of metazoans happened almost one billion year later in the mochim. Acta 236, 140–159. late Neoproterozoic. The simplest interpretation could be that un- Bartley, J.K., Kah, L.C., Frank, T.D., Lyons, T.W., 2015. Deep-water microbialites of the Mesoproterozoic Dismal Lakes Group: microbial growth, lithification, and stable or fluctuating O levels in the mid-Proterozoic may have 2 implications for coniform stromatolites. Geobiology 13, 15–32. served as a barrier for continuous evolution of eukaryotes (cf. Cox Bellefroid, E.J., Hood, A.V.S., Hoffman, P.F., Thomas, M.D., Reinhard, C.T., Planavsky, et al., 2018; Hardisty et al., 2017; Johnston et al., 2012). The exis- N.J., 2018. Constraints on Paleoproterozoic atmospheric oxygen levels. Proc. Natl. tence of a potentially large DOC reservoir and reduced iron pool Acad. Sci. 115, 8104–8109. in the ocean (ferruginous ocean) may have been the driver for Berner, R.A., Canfield, D.E., 1989. A new model for atmospheric oxygen over Phanerozoic time. Am. J. Sci. 289, 333–361. the overall anoxic surface environments in the Proterozoic—only Berner, R.A., Vandenbrooks, J.M., Ward, P.D., 2007. Oxygen and evolution. Sci- when the extra DOC and reduced iron in the ocean were largely ence 316, 557–558. removed through many pulses of oxidation, the surface ocean and Bjerrum, C.J., Canfield, D.E., 2011. Towards a quantitative understanding of the late Neoproterozoic carbon cycle. Proc. Natl. Acad. Sci. 108, 5542–5547. atmospheric O2 levels could become stable enough to support a Bristow, T.F., Kennedy, M.J., 2008. Carbon isotope excursions and the oxidant budget diversified eukaryotic ecosystem. of the Ediacaran atmosphere and ocean. Geology 36, 863–866. Butterfield, N.J., 2015. Early evolution of the Eukaryota. Palaeontology 58, 5–17. 6. Conclusions Canfield, D.E., Thamdrup, B., 2009. Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7, 385–392. High I/(Ca+Mg) ratios (≥2.6 μmol/mol; up to 3.4 μmol/mol) Canfield, D.E., Zhang, S., Frank, A.B., Wang, X., Wang, H., Su, J., Ye, Y., Frei, R., 2018. from the ca. 1.57–1.56 Ga shallow-water carbonates of the Highly fractionated chromium isotopes in Mesoproterozoic-aged shales and at- Gaoyuzhuang Formation in North China suggest a pulse of oxy- mospheric oxygen. Nat. Commun. 9, 2871. Cole, D.B., Reinhard, C.T., Wang, X., Gueguen, B., Halverson, G.P., Gibson, T., gen increase to ≥4% PAL. The increase of I/(Ca+Mg) ratios is Hodgskiss, M.S.W., McKenzie, N.R., Lyons, T.W., Planavsky, N.J., 2016. A shale- − h 13 13 accompanied by a 3.5 δ Ccarb and δ Corg anomaly and an hosted Cr isotope record of low atmospheric oxygen during the Proterozoic. increase in P/Al ratios that are best explained by the oxidation Geology 44, 555–558. M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797 15

Cox, G.M., Jarrett, A., Edwards, D., Crockford, P.W., Halverson, G.P., Collins, A.S., Formations, McArthur Basin, northern Australia. Geochim. Cosmochim. Acta 73, Poirier, A., Li, Z.X., 2016. Basin redox and primary productivity within the Meso- 2534–2558. proterozoic Roper Seaway. Chem. Geol. 440, 101–114. Knoll, A.H., 2014. Paleobiological perspectives on early eukaryotic evolution. Cold Cox, G.M., Lyons, T.W., Mitchell, R.N., Hasterok, D., Gard, M., 2018. Linking the rise Spring Harb. Perspect. Biol. 6, a016121. of atmospheric oxygen to growth in the continental phosphorus inventory. Earth Koehler, M.C., Stüeken, E.E., Kipp, M.A., Buick, R., Knoll, A.H., 2017. Spatial and tem- Planet. Sci. Lett. 489, 28–36. poral trends in Precambrian nitrogen cycling: a Mesoproterozoic offshore nitrate Crockford, P.W., Hayles, J.A., Bao, H., Planavsky, N.J., Bekker, A., Fralick, P.W., Halver- minimum. Geochim. Cosmochim. Acta 198, 315–337. son, G.P., Bui, T.H., Peng, Y., Wing, B.A., 2018. Triple oxygen isotope evidence for Kroeger, K.F., Funnell, R.H., 2012. Warm Eocene climate enhanced petroleum gener- limited mid-Proterozoic primary productivity. Nature 559, 613–616. ation from Cretaceous source rocks: a potential climate feedback mechanism? Crockford, P.W., Kunzmann, M., Bekker, A., Hayles, J., Bao, H., Halverson, G.P., Peng, Geophys. Res. Lett. 39, 3804. Y., Bui, T.H., Cox, G.M., Gibson, T.M., Wörndle, S., Rainbird, R., Lepland, A., Kump, L.R., 1991. Interpreting carbon-isotope excursions, Strangelove oceans. Geol- Swanson-Hysell, N.L., Master, S., Sreenivas, B., Kuznetsov, A., Krupenik, V., Wing, ogy 19, 299–302. B.A., 2019. Claypool continued: extending the isotopic record of sedimentary Li, H., Su, W., Zhou, H., Xiang, Z., Tian, H., Yang, L., Huff, W., Ettensohn, F., 2014. The sulfate. Chem. Geol. 513, 200–225. first precise age constraints on the Jixian System of the Meso- to Neoproterozoic Crowe, S.A., Døssing, L.N., Beukes, N.J., Bau, M., Kruger, S.J., Frei, R., Canfield, D.E., standard section of China: SHRIMP zircon U–Pb dating of bentonites from the 2013. Atmospheric oxygenation three billion years ago. Nature 501, 535. Wumishan and Tieling Formations in the Jixian section, North China Craton. Derry, L.A., 2010. A burial diagenesis origin for the Ediacaran Shuram-Wonoka car- Acta Petrol. Sin. 30, 2999–3012. bon isotope anomaly. Earth Planet. Sci. Lett. 294, 152–162. Li, H., Zhu, S., Xiang, Z., Su, W., Lu, S., Zhou, H., Geng, J., Li, S., Yang, F., 2010. Zir- Dickens, G.R., O’Neil, J.R., Rea, D.K., Owen, R.M., 1995. Dissociation of oceanic con U–Pb dating on tuff bed from Gaoyuzhuang Formation in Yanqing, Beijing: methane hydrate as a cause of the carbon isotope excursion at the end of the further constraints on the new subdivision of the Mesoproterozoic stratigraphy Paleocene. Paleoceanography 10, 965–971. in the northern North China Craton. Acta Petrol. Sin. 2, 2131–2140 (in Chinese Emerson, S., Cranston, R.E., Liss, P.S., 1979. Redox species in a reducing fjord: equi- with English abstract). librium and kinetic considerations. Deep-Sea Res., Part 1, Oceanogr. Res. Pap. 26, Li, R., Chen, J., Zang, S., Chen, Z., 2003. Secular variations in carbon isotopic compo- 859–878. sitions of carbonates from Proterozoic successions in the Ming Tombs Section of Farrenkopf, A.M., Luther III, G.W., 2002. Iodine chemistry reflects productivity and the North China Platform. J. Asian Earth Sci. 22, 329–341. denitrification in the Arabian Sea: evidence for flux of dissolved species from Liu, A., Tang, D., Shi, X., 2019, Zhou, Li, Zhou, X., Shang, M., Li, Y., Song, H. Growth sediments of western India into the OMZ. Deep-Sea Res., Part 2, Top. Stud. mechanisms and environmental implications of carbonate concretions from the Oceanogr. 49, 2303–2318. ∼1.4 Ga Xiamaling Formation, North China. J. Palaeogeogr. https://doi .org /10 . Farrenkopf, A.M., Luther III, G.W., Truesdale, V.W., Van Der Weijden, C.H., 1997. 1186 /s42501 -019 -0036 -4. Sub-surface iodide maxima: evidence for biologically catalyzed redox cycling in Lu, Z., Hoogakker, B.A., Hillenbrand, C.D., Zhou, X., Thomas, E., Gutchess, K.M., Lu, Arabian Sea OMZ during the SW intermonsoon. Deep-Sea Res., Part 2, Top. Stud. W., Jones, L., Rickaby, R.E.M., 2016. Oxygen depletion recorded in upper waters Oceanogr. 44, 1391–1409. of the glacial Southern Ocean. Nat. Commun. 7, 11146. Feng, X., Redfern, S.A., 2018. Iodate in calcite, aragonite and vaterite CaCO : in- 3 Lu, Z., Jenkyns, H.C., Rickaby, R.E., 2010. Iodine to calcium ratios in marine carbonate sights from first-principles calculations and implications for the I/Ca geochemi- as a paleo–redox proxy during oceanic anoxic events. Geology 38, 1107–1110. cal proxy. Geochim. Cosmochim. Acta 236, 351–360. Lu, W., Wörndle, S., Halverson, G.P., Zhou, X., Bekker, A., Rainbird, R.H., Hardisty, D.S., Gao, L., Ding, X., Gao, Q., Zhang, C., 2010. New geological time scale of Late Precam- Lyons, T.W., Lu, Z., 2017. Iodine proxy evidence for increased ocean oxygenation brian in China and geochronology. Geol. China 37, 1014–1020 (in Chinese with during the Bitter Springs Anomaly. Geochem. Perspect. Lett. 5, 53–57. English abstract). Lu, W., Ridgwell, A., Thomas, E., Hardisty, D.S., Luo, G., Algeo, T.J., Saltzman, M.R., Gao, L., Zhang, C., Liu, P., Ding, X., Wang, Z., Zhang, Y., 2009. Recognition of Meso- Gill, B.C., Shen, Y., Ling, H., Edwards, C.T., Whalen, M.T., Zhou, X., Gutchess, K.M., and Neoproterozoic stratigraphic framework in North and South China. Acta Jin, L., Rickaby, R.E.M., Jenkyns, H.C., Lyons, T.W., Lenton, T.M., Kump, L.R., Lu, Geosci. Sin. 30, 433–446 (in Chinese with English abstract). Z., 2018. Late inception of a resiliently oxygenated upper ocean. Science 361, Garcia, H.E., Locarnini, R.A., Boyer, T.P., Antonov, J.I., Mishonov, A.V., Baranova, O.K., 174–177. Zweng, M.M., Reagan, J.R., Johnson, D.R., 2013. Dissolved oxygen, apparent oxy- Luo, G., Junium, C., Kump, L., Huang, J., Li, C., Feng, Q., Shi, X., Bai, X., Xie, S., 2014. gen utilization, and oxygen saturation, vol. 13. In: Levitus, S. (Ed.), World Ocean Shallow stratification prevailed for ∼1700 to ∼1300 Ma ocean: evidence from Atlas 2013. NOAA Atlas NESDIS, vol. 75, pp. 1–27. organic carbon isotopes in the North China Craton. Earth Planet. Sci. Lett. 400, Gilleaudeau, G.J., Frei, R., Kaufman, A.J., Kah, L.C., Azmy, K., Bartley, J.K., Chernyavskiy, 219–232. P., Knoll, A.H., 2016. Oxygenation of the mid-Proterozoic atmosphere: clues from Luther III, G.W., Campbell, T., 1991. Iodine speciation in the water column of the chromium isotopes in carbonates. Geochem. Perspect. Lett. 2, 178–187. Black Sea. Deep-Sea Res., Part 1, Oceanogr. Res. Pap. 38, S875–S882. Glock, N., Liebetrau, V., Eisenhauer, A., 2014. I/Ca ratios in benthic foraminifera from Lyons, T.W., Reinhard, C.T., Planavsky, N.J., 2014. The rise of oxygen in Earth’s early the Peruvian oxygen minimum zone: analytical methodology and evaluation as ocean and atmosphere. Nature 506, 307–315. a proxy for redox conditions. Biogeosciences 11, 7077–7095. Guo, H., Du, Y., Kah, L.C., Huang, J., Hu, C., Huang, H., Yu, W., 2013. Isotopic compo- März, C., Poulton, S.W., Beckmann, B., Küster, K., Wagner, T., Kasten, S., 2008. Re- sition of organic and inorganic carbon from the Mesoproterozoic Jixian Group, dox sensitivity of P cycling during marine black shale formation: dynamics of North China: implications for biological and oceanic evolution. Precambrian sulfidic and anoxic, non-sulfidic bottom waters. Geochim. Cosmochim. Acta 72, Res. 224, 169–183. 3703–3717. Hardisty, D.S., Lu, Z., Bekker, A., Diamond, C.W., Gill, B.C., Jiang, G., Kah, L.C., Knoll, Mei, M., 2008. Sedimentary features and implications for the Precambrian non- A.H., Loyd, S.J., Osburn, M.R., Planavsky, N.J., Wang, C., Zhou, X., Lyons, T.W., stromatolitic carbonate succession: a case study of the Mesoproterozoic 2017. Perspectives on Proterozoic surface ocean redox from iodine contents in Gaoyuzhuang Formation at the Qiangou Section in Yanqing County of Beijing. ancient and recent carbonate. Earth Planet. Sci. Lett. 463, 159–170. Acta Geol. Sin. 82, 295–309 (English edition). Hardisty, D.S., Lu, Z., Planavsky, N.J., Bekker, A., Philippot, P., Zhou, X., Lyons, T.W., Mills, D.B., Ward, L.M., Jones, C., Sweeten, B., Forth, M., Treusch, A.H., Canfield, D.E., 2014. An iodine record of Paleoproterozoic surface ocean oxygenation. Geol- 2014. Oxygen requirements of the earliest animals. Proc. Natl. Acad. Sci. 111, ogy 42, 619–622. 4168–4172. Hemmingsson, C., Pitcairn, I.K., Fru, E.C., 2018. Evaluation of phosphate-uptake Mukherjee, I., Large, R.R., 2016. Pyrite trace element chemistry of the Velkerri For- mechanisms by Fe (III) (oxyhydr) oxides in Early Proterozoic oceanic conditions. mation, Roper Group, McArthur Basin: evidence for atmospheric oxygenation Environ. Chem. 15, 18–28. during the boring billion. Precambrian Res. 28, 13–26. Higgins, J.A., Blättler, C.L., Lundstrom, E.A., Santiago-Ramos, D.P., Akhtar, A.A., Crüger Mukherjee, I., Large, R.R., Corkrey, R., Danyushevsky, L.V., 2018. The Boring Billion, Ahm, A.-S., Bialik, O., Holmden, C., Bradbury, H., Murray, S.T., Swart, P.K., 2018. a slingshot for complex life on Earth. Sci. Rep. 8, 4432. https://doi .org /10 .1038 / Mineralogy, early marine diagenesis, and the chemistry of shallow-water car- s41598 -018 -22695 -x. bonate sediments. Geochim. Cosmochim. Acta 220, 512–534. Niu, S., 1998. Confirmation of the genus Grypania (megascopic alga) in Gaoyuzhuang Johnston, D., Poulton, S., Goldberg, T., Sergeev, V., Podkovyrov, V., Vorob’eva, N., Formation (1434 Ma) in Jixian (Tianjin) and its significance. Progress Precambr. Bekker, A., Knoll, A., 2012. Late Ediacaran redox stability and metazoan evo- Res. 21, 38–46 (In Chinese with English abstract). lution. Earth Planet. Sci. Lett. 335–336, 25–35. Oehlert, A.M., Swart, P.K., 2014. Interpreting carbonate and organic carbon isotope Kasting, J.F., 1991. Box models for the evolution of atmospheric oxygen: an up- covariance in the sedimentary record. Nat. Commun. 5, 4672. date. Palaeogeogr. Palaeoclimatol. Palaeoecol., Global Planet. Change Sect. 97, Olson, S.L., Kump, L.R., Kasting, J.F., 2013. Quantifying the areal extent and dissolved 125–131. oxygen concentrations of Archean oxygen oases. Chem. Geol. 362, 35–43. Kaufman, A.J., Corsetti, F.A., Varni, M.A., 2007. The effect of rising atmospheric oxy- Ozaki, K., Reinhard, C.T., Tajika, E., 2019. A sluggish mid-Proterozoic biosphere and gen on carbon and sulfur isotope anomalies in the Neoproterozoic Johnnie For- its effect on Earth’s redox balance. Geobiology 17, 3–11. mation, Death Valley, USA. Chem. Geol. 237, 47–63. Planavsky, N.J., McGoldrick, P., Scott, C.T., Li, C., Reinhard, C.T., Kelly, A.E., Chu, X., Kendall, B., Creaser, R.A., Gordon, G.W., Anbar, A.D., 2009. Re–Os and Mo isotope sys- Bekker, A., Love, G.D., Lyons, T.W., 2011. Widespread iron-rich conditions in the tematics of black shales from the Middle Proterozoic Velkerri and Wollogorang mid-Proterozoic ocean. Nature 477, 448. 16 M. Shang et al. / Earth and Planetary Science Letters 527 (2019) 115797

Planavsky, N.J., Reinhard, C.T., Wang, X., Thomson, D., McGoldrick, P., Rainhard, R.H., Tang, D., Shi, X., Jiang, G., Shi, Q., 2017b. Ferruginous seawater facilitates the trans- Johnson, T., Fischer, W.W., Lyons, T.W., 2014. Low Mid–Proterozoic atmospheric formation of glauconite to chamosite: an example from the Mesoproterozoic oxygen levels and the delayed rise of animals. Science 346, 635–638. Xiamaling Formation of North China. Am. Mineral. 102, 2317–2332. Planavsky, N.J., Slack, J.F., Cannon, W.F., O’Connell, B., Isson, T.T., Asael, D., Jackson, Tian, H., Zhang, J., Li, H., Su, W., Zhou, H., Yang, L., Xiang, Z., Geng, J., Liu, H., Zhu, J.C., Hardisty, D.S., Lyons, T.W., Bekker, A., 2018a. Evidence for episodic oxygena- S., Xu, Z., 2015. Zircon LA-MC-ICP-MS U–Pb dating of tuff from Mesoprotero- tion in a weakly redox-buffered deep mid-Proterozoic ocean. Chem. Geol. 483, zoic Gaoyuzhuang Formation in Jixian County of North China and its geological 581–594. significance. Acta Geosci. Sin. 36, 647–658 (in Chinese with English abstract). Planavsky, N.J., Cole, D.B., Isson, T.T., Reinhard, C.T., Crockford, P.W., Sheldon, N.D., Wang, H., Chu, X., Liu, B., Hou, H., Ma, L., 1985. Atlas of the Palaeogeography of Lyons, T.W., 2018b. A case for low atmospheric oxygen levels during Earth’s China. Cartographic Publishing House, Beijing (in Chinese and English, 143 pp.). middle history. Emerg. Top. Life Sci. 2, 149–159. Wang, X., Jiang, G., Shi, X., Peng, Y., Morales, D.C., 2018. Nitrogen isotope constraints Poulton, S.W., Canfield, D.E., 2011. Ferruginous conditions: a dominant feature of the on the early Ediacaran ocean redox structure. Geochim. Cosmochim. Acta 240, ocean through Earth’s history. Elements 7, 107–112. 220–235. Reinhard, C.T., Planavsky, N.J., Olson, S.L., Lyons, T.W., Erwin, D.H., 2016. Earth’s oxy- Wei, H., Wang, X., Shi, X., Jiang, G., Tang, D., 2019. Iodine content of the carbon- gen cycle and the evolution of animal life. Proc. Natl. Acad. Sci. 113, 8933–8938. ates from the Doushantuo Formation and shallow ocean redox change on the Reinhard, C.T., Planavsky, N.J., Gill, B.C., Ozaki, K., Robbins, L.J., Lyons, T.W., Fischer, Ediacaran Yangtze Platform, South China. Precambrian Res. 322, 160–169. W.W., Wang, C., Cole, D.B., Konhauser, K.O., 2017. Evolution of the global phos- Wörndle, S., Crockford, P.W., Kunzmann, M., Bui, T.H., Halverson, G.P., 2019. Linking phorus cycle. Nature 541, 386–389. the bitter springs carbon isotope anomaly and early Neoproterozoic oxygenation Rothman, D.H., Hayes, J.M., Summons, R.E., 2003. Dynamics of the Neoproterozoic through I/[Ca+Mg] ratios. Chem. Geol. https://doi .org /10 .1016 /j .chemgeo .2019 . carbon cycle. Proc. Natl. Acad. Sci. 100, 8124–8129. 06 .015. Rue, E.L., Smith, G.J., Cutter, G.A., Bruland, K.W., 1997. The response of trace element Yang, S., Kendall, B., Lu, X., Zhang, F., Zheng, W., 2017. Uranium isotope compo- redox couples to suboxic conditions in the water column. Deep-Sea Res., Part 1, sitions of mid-Proterozoic black shales: evidence for an episode of increased Oceanogr. Res. Pap. 44, 113–134. ocean oxygenation at 1.36 Ga and evaluation of the effect of post-depositional Runnegar, B., 1991. Precambrian oxygen levels estimated from the biochemistry and hydrothermal fluid flow. Precambrian Res. 298, 187–201. physiology of early eukaryotes. Palaeogeogr. Palaeoclimatol. Palaeoecol., Global Zbinden, E.A., Holland, H.D., Feakes, C.R., Dobos, S.K., 1988. The Sturgeon Falls pa- Planet. Change Sect. 97, 97–111. leosol and the composition of the atmosphere 1.1 Ga BP. Precambrian Res. 42, Rye, R., Holland, H.D., 1998. Paleosols and the evolution of atmospheric oxygen: a 141–163. critical review. Am. J. Sci. 298, 621–672. Zhang, K., Zhu, X., Wood, R.A., Shi, Y., Gao, Z., Poulton, S.W., 2018. Oxygenation Schrag, D.P., Higgins, J.A., Macdonald, F.A., Johnston, D.T., 2013. Authigenic carbonate of the Mesoproterozoic ocean and the evolution of complex eukaryotes. Nat. and the history of the global carbon cycle. Science 339, 540–543. Geosci. https://doi .org /10 .1038 /s41561 -018 -0111 -y. Sperling, E.A., Halverson, G.P., Knoll, A.H., Macdonald, F.A., Johnston, D.T., 2013. A Zhang, S., Wang, X., Wang, H., Bjerrum, C.J., Hammarlund, E.U., Costa, M.M., Connelly, basin redox transect at the dawn of animal life. Earth Planet. Sci. Lett. 371, J.N., Zhang, B., Su, J., Canfield, D.E., 2016. Sufficient oxygen for animal respiration 143–155. 1,400 million years ago. Proc. Natl. Acad. Sci. 113, 1731–1736. Sperling, E.A., Wolock, C.J., Morgan, A.S., Gill, B.C., Kunzmann, M., Halverson, Zhang, S., Wang, X., Wang, H., Hammarlund, E.U., Su, J., Wang, Y., Canfield, D.E., G.P., Macdonald, F.A., Knoll, A., Johnston, D., 2015. Statistical analysis of iron 2017. The oxic degradation of sedimentary organic matter 1400 Ma constrains geochemical data suggests limited late Proterozoic oxygenation. Nature 523, atmospheric oxygen levels. Biogeosciences 14, 2133–2149. 451–454. Zhang, S., Wang, X., Hammarlund, E.U., Wang, H., Costa, M.M., Bjerrum, C.J., Connelly, Sperling, E.A., Rooney, A.D., Hays, L., Sergeev, V.N., Vorob’Eva, N.G., Sergeeva, N.D., J.N., Zhang, B., Bian, L., Canfield, D.E., 2015. Orbital forcing of climate 1.4 billion Selby, D., Johnston, D.T., Knoll, A.H., 2014. Redox heterogeneity of subsurface years ago. Proc. Natl. Acad. Sci. 112, E1406–E1413. waters in the Mesoproterozoic ocean. Geobiology 12, 373–386. Zhang, W., Shi, X., Tang, D., Wang, X., 2016. The characteristic and genetic in- Su, W., Li, H., Huff, W., Ettensohn, F., Zhang, S., Zhou, H., Wan, Y., 2010. SHRIMP terpretation of thrombolite in Mesoproterozoic Gaoyuzhuang Formation from U–Pb dating for a K-bentonite bed in the Tieling Formation, North China. Chin. Pingquan, Hubei Province. Chin. J. Geol. 51, 1324–1343 (in Chinese with English Sci. Bull. 55, 3312–3323. abstract). Sun, S., Zhu, S., Huang, X., 2006. Discovery of megafossils from the Mesoproterozoic Zhao, X., Wang, X., Shi, X., Tang, D., Shi, Q., 2018. Stepwise oxygenation of early Gaoyuzhuang Formation in the Jixian Section, Tianjin and its stratigraphic sig- Cambrian ocean controls early metazoan diversification. Palaeogeogr. Palaeocli- nificance. Acta Palaeontol. Sin. 45, 207–220 (in Chinese with English abstract). matol. Palaeoecol. 504, 86–103. 13 Swart, P.K., Eberli, G., 2005. The nature of the δ Cof periplatform sediments: im- Zhou, X., Jenkyns, H.C., Lu, W., Hardisty, D.S., Owens, J.D., Lyons, T.W., Lu, Z., 2017. plications for stratigraphy and the global carbon cycle. Sediment. Geol. 175, Organically bound iodine as a bottom-water redox proxy: preliminary validation 115–129. and application. Chem. Geol. 457, 95–106. Swart, P.K., 2008. Global synchronous changes in the carbon isotopic composition of Zhou, X., Jenkyns, H.C., Owens, J.D., Junium, C.K., Zheng, X., Sageman, B.B., Hardisty, carbonate sediments unrelated to changes in the global carbon cycle. Proc. Natl. D.S., Lyons, T.W., Ridgwell, A., Lu, Z., 2015. Upper ocean oxygenation dynamics Acad. Sci. 70, 738–748. from I/Ca ratios during the Cenomanian–Turonian OAE 2. Paleoceanography 30, Tang, D., Shi, X., Wang, X., Jiang, G., 2016. Extremely low oxygen concentration in 510–526. mid-Proterozoic shallow seawaters. Precambrian Res. 276, 145–157. Zhou, X., Thomas, E., Rickaby, R.E.M., Winguth, A.M., Lu, Z., 2014. I/Ca evidence for Tang, D., Shi, X., Jiang, G., 2013. Mesoproterozoic biogenic thrombolites from the upper ocean deoxygenation during the PETM. Paleoceanography 29, 964–975. North China Platform. Int. J. Earth Sci. 102, 401–413. Zhu, S., Zhu, M., Knoll, A.H., Yin, Z., Zhao, F., Sun, S., Qu, Y., Shi, M., Liu, H., Tang, D., Shi, X., Zhang, W., Liu, Y., Wu, J., 2017a. Mesoproterozoic herringbone cal- 2016. Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old cite from North China Platform: genesis and paleoenvirnmental significance. J. Gaoyuzhuang Formation in North China. Nat. Commun. 7, 11500. Paleogeogr. 19, 227–240 (in Chinese with English abstract).