Corrected: Publisher correction ARTICLE DOI: 10.1038/s41467-018-04980-5 OPEN Coupling of ocean redox and animal evolution during the Ediacaran-Cambrian transition Dan Wang1,2, Hong-Fei Ling2, Ulrich Struck3,4, Xiang-Kun Zhu1, Maoyan Zhu5,6, Tianchen He7, Ben Yang8, Antonia Gamper3,4 & Graham A. Shields 9 The late Ediacaran to early Cambrian interval witnessed extraordinary radiations of metazoan life. The role of the physical environment in this biological revolution, such as changes to 1234567890():,; oxygen levels and nutrient availability, has been the focus of longstanding debate. Seemingly contradictory data from geochemical redox proxies help to fuel this controversy. As an essential nutrient, nitrogen can help to resolve this impasse by establishing linkages between nutrient supply, ocean redox, and biological changes. Here we present a comprehensive N- isotope dataset from the Yangtze Basin that reveals remarkable coupling between δ15N, δ13C, and evolutionary events from circa 551 to 515 Ma. The results indicate that increased fixed nitrogen supply may have facilitated episodic animal radiations by reinforcing ocean oxy- genation, and restricting anoxia to near, or even at the sediment–water interface. Conversely, sporadic ocean anoxic events interrupted ocean oxygenation, and may have led to extinctions of the Ediacaran biota and small shelly animals. 1 MNR Key Laboratory of Isotope Geology, MNR Key Laboratory of Deep-Earth Dynamics, Institute of Geology, Chinese Academy of Geological Sciences, Beijing 100037, China. 2 State Key Laboratory for Mineral Deposits Research, School of Earth Sciences and Engineering, Nanjing University, Nanjing 210023, China. 3 Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany. 4 Department of Earth Sciences, Freie Universität Berlin, Malteserstrasse 74-100, Haus D, 12249 Berlin, Germany. 5 State Key Laboratory of Palaeobiology and Stratigraphy, Center for Excellence in Life and Paleoenvironment, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 210008 Nanjing, China. 6 College of Earth Sciences, University of Chinese Academy of Sciences, 100049 Beijing, China. 7 School of Earth and Environment, University of Leeds, Leeds LS2 9JT, UK. 8 MNR Key Laboratory of Stratigraphy and Palaeontology, Institute of Geology, Chinese Academy of Geological Sciences, 100037 Beijing, China. 9 Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK. Correspondence and requests for materials should be addressed to D.W. (email: [email protected]) or to H.-F.L. (email: hfl[email protected]) NATURE COMMUNICATIONS | (2018) 9:2575 | DOI: 10.1038/s41467-018-04980-5 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-04980-5 – oft-bodied macroscopic multicellular Ediacara organisms, evolution11 14. However, iron speciation data also suggest a high including animals, appeared abruptly in the fossil records degree of redox heterogeneity, and possibly even dominantly S 1 during the late Ediacaran Period , and were then replaced anoxic conditions with scant measurable change in oxygenation – by bilaterian and biomineralized animals in ecosystems, which through the Ediacaran to Cambrian interval15 17. A new model approached modern levels of complexity by the early Cambrian2. for ocean redox is, therefore, required to resolve these seemingly The underlying causes for biodiversification and bioradiations contradictory datasets, in particular where a direct relationship during the Ediacaran and early Cambrian are still controversial3. between animal radiation and extinction events can be The key innovations in complex animals during the established. Ediacaran–Cambrian transition interval were skeletonization4, The N isotopic composition of marine sediments has great motility5, predation6, large body size, and complex food webs1,2. potential to provide clues about ocean redox structure and its While some simple animals, such as soft-bodied sponges, which direct links with bio-evolution18. The marine nitrogen cycle is may have their origins in the Tonian7, could have had low oxygen driven by metabolic pathways that exhibit differing isotopic requirements (0.5–4.0% of present-day levels)8, macroscopic fractionations19. Nitrogen enters the oceanic N cycle mainly – fi fi animals of the Ediacaran Cambrian transition likely required through the xation of atmospheric N2 (N2- xation) by auto- oxygen levels above the physiological thresholds for those ener- trophs using Mo-nitrogenases with minor isotopic fractionation getically expensive behaviors9,10. A gradual rise in oceanic oxygen (≤2‰)19. This process requires high energy to break the mole- levels has been proposed based on substantial geochemical evi- cular nitrogen bond, and can only be performed by some bacteria dence, e.g., the high abundance and isotope values of redox- and archaea20. Denitrification and anaerobic ammonia oxidation sensitive trace metals (Mo and U) in euxinic sediments, and (i.e., anammox) release nitrogen back to the atmosphere as indeed seems to occur contemporaneously with animal nitrous oxide (N2O) or N2, and are the largest sinks of nitrogen b Xi’an North China Platform Nanjing Shanghai Yichang Wuhan Chengdu N 2 9 Chongqing 6 Changsha 7 Uplift Uplift 1 3 8 Guiyang 4 Uplift Uplift Kunming 5 Yangzte Taiwan Guangzhou Cathaysia Nanning a Hongkong Vietnam Transition zone Laos (carbonate/shale) Platform Slope/basin Hainan (carbonate) (mudstone/chert) c Xi’an North China Platform Upper Yangtze region Nanjing 1. Xiaotan section, Yunan Shanghai 2. Sancha section, Hunan Yichang Wuhan 3. Zhongnan section, Guizhou Chengdu 9 4. Nangao section, Guizhou 2 Chongqing 5. Zhalagou section, Guizhou 6 Changsha 7 Uplift Uplift 1 3 6. Longbizui section, Hunan 8 7. Lijiatuo section, Hunan Guiyang 4 8. Yuanjia section, Hunan Uplift Uplift Kunming 5 Lower Yangtze region 9. Yanjia, section, Zhejiang Taiwan Guangzhou Nanning Hongkong Vietnam Shale/sandstone Laos 300 km 600 km Hainan 0 Fig. 1 Tectonic setting and simplified geological map of the Yangtze block during the late Ediacaran–early Cambrian. a Tectonic setting of South China. b Simplified geological map of the Yangtze block during the late Ediacaran to Cambrian Fortunian Stage, and c during Cambrian Stage 2 (modified after ref. 24) 2 NATURE COMMUNICATIONS | (2018) 9:2575 | DOI: 10.1038/s41467-018-04980-5 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-04980-5 ARTICLE from the ocean19. These processes only occur under oxygen- evolution across the Ediacaran–Cambrian transition, remain deficient conditions, with significant fractionations of ~ 20–30‰ poorly understood. in the water column, but with negligible fractionation in the Late Ediacaran to Cambrian successions are both fossiliferous sediments19,21. The balance between nitrogen fixation and deni- and well developed along the Yangtze continental margin, South trification/anammox ultimately governs the fixed inorganic China, providing an excellent opportunity to conduct a com- nitrogen reservoir in the ocean and its isotopic composition19.As prehensive study of nitrogen isotopes (Fig. 1). This study presents it is a principal nutrient for life, nitrogen, by way of its redox a comprehensive curve of new and published δ15N data from nine sensitivity is considered to be an important control on the sections representing different depositional facies across South growth of eukaryotic producers and primary productivity22. China. Our results demonstrate regional redox fluctuations However, nitrogen abundance and speciation, as well as its rela- against the background of a generally well-oxygenated open tionship with ocean redox state, productivity and animal ocean. We find that ocean redox dynamics were closely coupled a Extinction of Exinction of small shelly fossils Ediacaran-type biota Chengjiang faunaSmall shelly fossils Ediacaran biota 8 b SHICE BACE 4 0 (‰) -4 carb DEPCE C –8 13 δ CARE –12 ZHUCE –16 c –24 –28 (‰) org –32 C 13 δ –36 –40 d Interval 8 IV 6 4 2 0 N(‰) 15 –2 δ Interval III Interval I –4 Interval Interval VI V Interval –6 II –8 ? Stage 3 Stage 2 Fortunian Ediacaran 515 521 528 542 551 Million-years ago Nitrate-based production as in modern ocean Upper Yangtze region, South China Lower Yangtze region, South China Xiaotan Platform Nangao Slope Yanjia Slope-basin Sancha Shelf margin Longbizui Slope Zhongnan Shelf margin Lijiatuo Slope-basin Platform, Kazakhstan Zhalagou Slope Yuanjia Basin Kyrshabakty & Berkuty sections 13 13 15 Fig. 2 Compilation of δ Ccarb, δ Corg, and δ N data with evolutionary events during the late Ediacaran–early Cambrian. a Key bioevents during the late 31 13 13 Ediacaran–early Cambrian proposed by ref. b δ Ccarb profile from the Xiaotan section (Yunnan) on the Yangtze platform. δ Ccarb data are from refs. 67,68. DEPCE: DEngying Positive Carbon isotope Excursion, BACE: Basal Cambrian Carbon isotope Excursion, ZHUCE: Zhujiaqing Carbon isotope Excursion, 31 13 SHICE: Shiyantou Carbon isotope Excursion, CARE: Cambrian Arthropod Radiation isotope Excursion . c Compiled δ Corg curve for nine sections in 13 26,28–30,69–71 15 various depositional facies on the Yangtze block. Corg data are from this study and refs. d Compiled δ N profile for nine sections in various depositional facies on the Yangtze block and two sections in the Malyi Karatau area of the southern Kazakhstan. δ15N data are from this study and 26–30,63 13 13 15 refs. The mean long-term trends of