Nitrogen Isotopes from the Neoproterozoic Liulaobei Formation, North China: Implications for Nitrogen Cycling and Eukaryotic Evolution

Abstract

The nitrogen isotope compositions (δ¹⁵N) of sedimentary rocks can provide information about the nutrient N cycling and redox conditions that may have played important roles in biological evolution in Earth’s history. Although considerable δ¹⁵N data for the Precambrian have been published, there is a large gap during the Early Neoproterozoic that restrains our understanding of the linkages among N cycling, ocean redox changes and biological evolution during this key period. Here, we report bulk δ¹⁵N and organic carbon isotope (δ,¹³C_org) compositions as well as the total nitrogen (TN) and total organic carbon (TOC) contents from the Tonian fossiliferous Liulaobei Formation in the southern part of the North China Platform. The δ¹⁵N in the study section is dominated by very stable values centering around +4.3‰, which is moderately lower than that in modern sediments (∼+6‰). These positive δ¹⁵N values were attributed to partial denitrification under low primary productivity (scenario 1) and/or denitrification coupled with dissimilatory nitrate reduction to ammonium (DNRA) (scenario 2). In either case, the availability of fixed nitrogen may have provided the nutrient N required to facilitate facilitated eukaryotic growth. Our study highlights the pivotal role of nutrient N in the evolution of eukaryotes.

Keywords

Neoproterozoic / Tonian / Liulaobei Formation / nitrogen isotopes / eukaryotic evolution / nutrient limitation / geochemistry

References

Ader M, Macouin M, Trindade R I F, . A Multilayered Water Column in the Ediacaran Yangtze Platform? Insights from Carbonate and Organic Matter Paired δ¹³C. Earth and Planetary Science Letters, 2009, 288(1/2): 213-227.

Ader M, Sansjofre P, Halverson G P, . Ocean Redox Structure across the Late Neoproterozoic Oxygenation Event: A Nitrogen Isotope Perspective. Earth and Planetary Science Letters, 2014, 396: 1-13.

Ader M, Thomazo C, Sansjofre P, . Interpretation of the Nitrogen Isotopic Composition of Precambrian Sedimentary Rocks: Assumptions and Perspectives. Chemical Geology, 2016, 429: 93-110.

Algeo T J, Meyers P A, Robinson R S, . Icehouse-Greenhouse Variations in Marine Denitrification. Biogeosciences, 2014, 11(4): 1273-1295.

Altabet M A, Pilskaln C, Thunell R, . The Nitrogen Isotope Biogeochemistry of Sinking Particles from the Margin of the Eastern North Pacific. Deep Sea Research Part I: Oceanographic Research Papers, 1999, 46(4): 655-679.

Altabet M A. Volkman J K. Isotopic Tracers of the Marine Nitrogen Cycle: Present and Past. Marine Organic Matter: Biomarkers, Isotopes and DNA, 2006, Berlin Heidelberg: Springer

Bristow L A, Dalsgaard T, Tiano L, . Ammonium and Nitrite Oxidation at Nanomolar Oxygen Concentrations in Oxygen Minimum Zone Waters. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(38): 10601-10606.

Canfield D E, Zhang S, Frank A B, . Highly Fractionated Chromium Isotopes in Mesoproterozoic-Aged Shales and Atmospheric Oxygen. Nature Communications, 2018, 9 2871

Chang C, Hu W X, Wang X L, . Nitrogen Isotope Evidence for an Oligotrophic Shallow Ocean during the Cambrian Stage 4. Geochimica et Cosmochimica Acta, 2019, 257: 49-67.

Chen Y, Diamond C W, Stüeken E E, . Coupled Evolution of Nitrogen Cycling and Redoxcline Dynamics on the Yangtze Block across the Ediacaran — Cambrian Transition. Geochimica et Cosmochimica Acta, 2019, 257: 243-265.

Cole D B, Reinhard C T, Wang X L, . A Shale-Hosted Cr Isotope Record of Low Atmospheric Oxygen during the Proterozoic. Geology, 2016, 44(7): 555-558.

Crockford P W, Kunzmann M, Bekker A, . Claypool Continued: Extending the Isotopic Record of Sedimentary Sulfate. Chemical Geology, 2019, 513: 200-225.

Diamond C W, Planavsky N J, Wang C, . What the ∼1.4 Ga Xiamaling Formation can and Cannot Tell Us about the Mid-Proterozoic Ocean. Geobiology, 2018, 16(3): 219-236.

Dong L, Xiao S H, Shen B, . Restudy of the Worm-Like Carbonaceous Compression Fossils Protoarenicola, Pararenicola, and Sinosabellidites from Early Neoproterozoic Successions in North China. Palaeogeography, Palaeoclimatology, Palaeoecology, 2008, 258(3): 138-161.

Freudenthal T, Wagner T, Wenzhöfer F, . Early Diagenesis of Organic Matter from Sediments of the Eastern Subtropical Atlantic: Evidence from Stable Nitrogen and Carbon Isotopes. Geochimica et Cosmochimica Acta, 2001, 65(11): 1795-1808.

Fuchsman C A, Murray J W, Konovalov S K. Concentration and Natural Stable Isotope Profiles of Nitrogen Species in the Black Sea. Marine Chemistry, 2008, 111(1/2): 90-105.

Giblin A, Tobias C, Song B, . The Importance of Dissimilatory Nitrate Reduction to Ammonium (DNRA) in the Nitrogen Cycle of Coastal Ecosystems. Oceanography, 2013, 26(3): 124-131.

Godfrey L V, Poulton S W, Bebout G E, . Stability of the Nitrogen Cycle during Development of Sulfidic Water in the Redox-Stratified Late Paleoproterozoic Ocean. Geology, 2013, 41(6): 655-658.

Guilbaud R, Poulton S W, Thompson J, . Phosphorus-Limited Conditions in the Early Neoproterozoic Ocean Maintained Low Levels of Atmospheric Oxygen. Nature Geoscience, 2020, 13: 296-301.

Guilbaud R, Poulton S W, Butterfield N J, . A Global Transition to Ferruginous Conditions in the Early Neoproterozoic Oceans. Nature Geoscience, 2015, 8: 466-470.

Hayes J M, Strauss H, Kaufman A J. The Abundance of ¹³C in Marine Organic Matter and Isotopic Fractionation in the Global Biogeochemical Cycle of Carbon during the Past 800 Ma. Chemical Geology, 1999, 161(1/2/3): 103-125.

Higgins M B, Robinson R S, Husson J M, . Dominant Eukaryotic Export Production during Ocean Anoxic Events Reflects the Importance of Recycled NH₄. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(7): 2269-2274.

Hong T, Jia Z, Yin L, . Acritarchs from the Neoproterozoic Jiuliqiao Formation, Huainan Region, and Their Biostratigraphic Significance. Acta Palaeontologica Sinica, 2004, 43: 377-387.

Jiang G Q, Wang X Q, Shi X Y, . The Origin of Decoupled Carbonate and Organic Carbon Isotope Signatures in the Early Cambrian (ca. 542–520 Ma) Yangtze Platform. Earth and Planetary Science Letters, 2012, 317/318: 96-110.

Kipp M A, Stüeken E E, Yun M, . Pervasive Aerobic Nitrogen Cycling in the Surface Ocean across the Paleoproterozoic Era. Earth and Planetary Science Letters, 2018, 500: 117-126.

Knoll A H, Nowak M A. The Timetable of Evolution. Science Advances, 2017, 3 5 e1603076

Koehler M C, Stüeken E E, Kipp M A, . Spatial and Temporal Trends in Precambrian Nitrogen Cycling: A Mesoproterozoic Offshore Nitrate Minimum. Geochimica et Cosmochimica Acta, 2017, 198: 315-337.

Lam P, Kuypers M M M. Microbial Nitrogen Cycling Processes in Oxygen Minimum Zones. Annual Review of Marine Science, 2011, 3: 317-345.

Lan Z W, Zhang S J, Tucker M, . Evidence for Microbes in Early Neoproterozoic Stromatolites. Sedimentary Geology, 2020, 398 105589

Lehmann M F, Bernasconi S M, Barbieri A, . Preservation of Organic Matter and Alteration of Its Carbon and Nitrogen Isotope Composition during Simulated and in situ Early Sedimentary Diagenesis. Geochimica et Cosmochimica Acta, 2002, 66(20): 3573-3584.

Li G J, Chen L, Pang K, . An Assemblage of Macroscopic and Diversified Carbonaceous Compression Fossils from the Tonian Shiwangzhuang Formation in Western Shandong, North China. Precambrian Research, 2020, 346 105801

Lu W, Wörndle S, Halverson G P, . Iodine Proxy Evidence for Increased Ocean Oxygenation during the Bitter Springs Anomaly. Geochemical Perspectives Letters, 2017, 5: 53-57.

Luo G M, Junium C K, Kump L R, . Shallow Stratification Prevailed for ∼ 1 700 to ∼ 1 300 Ma Ocean: Evidence from Organic Carbon Isotopes in the North China Craton. Earth and Planetary Science Letters, 2014, 400: 219-232.

Luo G M, Wang Y B, Algeo T J, . Enhanced Nitrogen Fixation in the Immediate Aftermath of the Latest Permian Marine Mass Extinction. Geology, 2011, 39(7): 647-650.

Luo G M, Junium C K, Izon G, . Nitrogen Fixation Sustained Productivity in the Wake of the Palaeoproterozoic Great Oxygenation Event. Nature Communications, 2018, 9 978

Lyons T W, Reinhard C T, Planavsky N J. The Rise of Oxygen in Earth’s Early Ocean and Atmosphere. Nature, 2014, 506: 307-315.

MacDonald F A, Schmitz M D, Crowley J L, . Calibrating the Cryogenian. Science, 2010, 327(5970): 1241-1243.

McCready R G L, Gould W D, Barendregt R W. Nitrogen Isotope Fractionation during the Reduction of NO₃ ⁻ to NH₄ by Desulfovibrio Sp. Canadian Journal of Microbiology, 1983, 29(2): 231-234.

Michiels C C, Darchambeau F, Roland F A E, . Iron-Dependent Nitrogen Cycling in a Ferruginous Lake and the Nutrient Status of Proterozoic Oceans. Nature Geoscience, 2017, 10 217

Morales L V, Granger J, Chang B X, . Elevated ¹⁵N/¹⁴N in Particulate Organic Matter, Zooplankton, and Diatom Frustule-Bound Nitrogen in the Ice-Covered Water Column of the Bering Sea Eastern Shelf. Deep Sea Research Part II: Topical Studies in Oceanography, 2014, 109: 100-111.

Ossa O F, Hofmann A, Spangenberg J E, . Limited Oxygen Production in the Mesoarchean Ocean. Proceedings of the National Academy of Sciences of the United States of America, 2019, 116(14): 6647-6652.

Pang K, Tang Q, Chen L, . Nitrogen-Fixing Heterocystous Cyanobacteria in the Tonian Period. Current Biology, 2018, 28(4): 616-622.e1.

Papineau D, Purohit R, Goldberg T, . High Primary Productivity and Nitrogen Cycling after the Paleoproterozoic Phosphogenic Event in the Aravalli Supergroup, India. Precambrian Research, 2009, 171(1/2/3/4): 37-56.

Planavsky N J. The Elements of Marine Life. Nature Geoscience, 2014, 7: 855-856.

Planavsky N J, Cole D B, Reinhard C T, . No Evidence for High Atmospheric Oxygen Levels 1 400 Million Years Ago. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(19): E2550-E2551.

Planavsky N J, Reinhard C T, Wang X, . Low Mid-Proterozoic Atmospheric Oxygen Levels and the Delayed Rise of Animals. Science, 2014, 346(6209): 635-638.

Planavsky N J, McGoldrick P, Scott C T, . Widespread Iron-Rich Conditions in the Mid-Proterozoic Ocean. Nature, 2011, 477: 448-451.

Poulton S W, Canfield D E. Ferruginous Conditions: A Dominant Feature of the Ocean through Earth’s History. Elements, 2011, 7(2): 107-112.

Prokopenko M G, Hammond D E, Berelson W M, . Nitrogen Cycling in the Sediments of Santa Barbara Basin and Eastern Subtropical North Pacific: Nitrogen Isotopes, Diagenesis and Possible Chemosymbiosis between Two Lithotrophs (Thioploca and Anammox) — “Riding on a Glider”. Earth and Planetary Science Letters, 2006, 242(1/2): 186-204.

Reinhard C T, Planavsky N J, Gill B C, . Evolution of the Global Phosphorus Cycle. Nature, 2017, 541: 386-389.

Reinhard C T, Planavsky N J, Robbins L J, . Proterozoic Ocean Redox and Biogeochemical Stasis. PNAS, 2013, 110(14): 5357-5362.

Riedman L A, Sadler P M. Global Species Richness Record and Biostratigraphic Potential of Early to Middle Neoproterozoic Eukaryote Fossils. Precambrian Research, 2018, 319: 6-18.

Robinson R S, Kienast M, Luiza Albuquerque A, . A Review of Nitrogen Isotopic Alteration in Marine Sediments. Paleoceanography, 2012, 27 4 PA4203

Rooney A D, MacDonald F A, Strauss J V, . Re-Os Geochronology and Coupled Os−Sr Isotope Constraints on the Sturtian Snowball Earth. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(1): 51-56.

Sahoo S K, Planavsky N J, Kendall B, . Ocean Oxygenation in the Wake of the Marinoan Glaciation. Nature, 2012, 489: 546-549.

Scott C, Lyons T W, Bekker A, . Tracing the Stepwise Oxygenation of the Proterozoic Ocean. Nature, 2008, 452: 455-456.

Shang M H, Tang D J, Shi X Y, . A Pulse of Oxygen Increase in the Early Mesoproterozoic Ocean at ca. 1.57–1.56 Ga. Earth and Planetary Science Letters, 2019, 527 115797

Shen B, Xiao S H, Zhou C M, . Carbon and Sulfur Isotope Chemostratigraphy of the Neoproterozoic Quanji Group of the Chaidam Basin, NW China: Basin Stratification in the Aftermath of an Ediacaran Glaciation Postdating the Shuram Event. Precambrian Research, 2010, 177(3/4): 241-252.

Sigman D M, Karsh K L, Casciotti K L. Ocean Process Tracers: Nitrogen Isotopes in the Ocean, 2009, Amsterdam: In: Encyclopedia of Ocean Sciences, Elsevier

Stüeken E E. A Test of the Nitrogen-Limitation Hypothesis for Retarded Eukaryote Radiation: Nitrogen Isotopes across a Mesoproterozoic Basinal Profile. Geochimica et Cosmochimica Acta, 2013, 120: 121-139.

Stüeken E E, Buick R, Guy B M, . Isotopic Evidence for Biological Nitrogen Fixation by Molybdenum-Nitrogenase from 3.2 Gyr. Nature, 2015, 520: 666-669.

Stüeken E E, Buick R, Lyons T W. Revisiting the Depositional Environment of the Neoproterozoic Callanna Group, South Australia. Precambrian Research, 2019, 334 105474

Stüeken E E, Kipp M A, Koehler M C, . The Evolution of Earth’s Biogeochemical Nitrogen Cycle. Earth-Science Reviews, 2016, 160: 220-239.

Sun W G, Wang G X, Zhou B H. Macroscopic Worm-Like Body Fossils from the Upper Precambrian (900–700 Ma), Huainan District, Anhui, China and Their Stratigraphic and Evolutionary Significance. Precambrian Research, 1986, 31(4): 377-403.

Tang Q, Pang K, Xiao S H, . Organic-Walled Microfossils from the Early Neoproterozoic Liulaobei Formation in the Huainan Region of North China and Their Biostratigraphic Significance. Precambrian Research, 2013, 236: 157-181.

Tang Q, Pang K, Yuan X L, . Electron Microscopy Reveals Evidence for Simple Multicellularity in the Proterozoic Fossil Chuaria. Geology, 2017, 45(1): 75-78.

Tang Q, Pang K, Yuan X, . A One-Billion-Year-Old Multicellular Chlorophyte. Nature Ecology & Evolution, 2020, 4: 543-549.

Thomazo C, Ader M, Philippot P. Extreme ¹⁵N-Enrichments in 2.72-Gyr-Old Sediments: Evidence for a Turning Point in the Nitrogen Cycle. Geobiology, 2011, 9(2): 107-120.

Thomson D, Rainbird R H, Planavsky N, . Chemostratigraphy of the Shaler Supergroup, Victoria Island, NW Canada: A Record of Ocean Composition Prior to the Cryogenian Glaciations. Precambrian Research, 2015, 263: 232-245.

Thunell R C, Sigman D M, Muller-Karger F, . Nitrogen Isotope Dynamics of the Cariaco Basin, Venezuela. Global Biogeochemical Cycles, 2004, 18 3 GB3001

Turner E C, Bekker A. Thick Sulfate Evaporite Accumulations Marking a Mid-Neoproterozoic Oxygenation Event (Ten Stone Formation, Northwest Territories, Canada). Geological Society of America Bulletin, 2016, 128(1/2): 203-222.

Tyrrell T. The Relative Influences of Nitrogen and Phosphorus on Oceanic Primary Production. Nature, 1999, 400: 525-531.

Wang D, Ling H-F, Struck U, . Coupling of Ocean Redox and Animal Evolution during the Ediacaran-Cambrian Transition. Nature Communications, 2018, 9 2575

Wang G, Zhang S, Li S, . Research on the Upper Precambrian of Northern Jiangsu and Anhui Provinces, 1984, Hefei: Anhui Press of Science and Technology

Wang H Y, Zhang Z H, Li C, . Spatiotemporal Redox Heterogeneity and Transient Marine Shelf Oxygenation in the Mesoproterozoic Ocean. Geochimica et Cosmochimica Acta, 2020, 270: 201-217.

Wang X Q, Jiang G Q, Shi X Y, . Nitrogen Isotope Constraints on the Early Ediacaran Ocean Redox Structure. Geochimica et Cosmochimica Acta, 2018, 240: 220-35.

Wang X Q, Shi X Y, Tang D J, . Nitrogen Isotope Evidence for Redox Variations at the Ediacaran-Cambrian Transition in South China. The Journal of Geology, 2013, 121(5): 489-502.

Wang Z P, Wang X Q, Shi X Y, . Coupled Nitrate and Phosphate Availability Facilitated the Expansion of Eukaryotic Life at Circa 1.56 Ga. Journal of Geophysical Research: Biogeosciences, 2020, 125 4 e2019JG005487.

Xiao S H, Bao H M, Wang H F, . The Neoproterozoic Quruqtagh Group in Eastern Chinese Tianshan: Evidence for a Post-Marinoan Glaciation. Precambrian Research, 2004, 130(1/2/3/4): 1-26.

Xiao S H, Shen B, Tang Q, . Biostratigraphic and Chemostratigraphic Constraints on the Age of Early Neoproterozoic Carbonate Successions in North China. Precambrian Research, 2014, 246: 208-225.

Xiao S H, Tang Q. After the Boring Billion and before the Freezing Millions: Evolutionary Patterns and Innovations in the Tonian Period. Emerging Topics in Life Sciences, 2018, 2(2): 161-171.

Xing Y. The Upper Precambrian of China, Volume 3 of “The Stratigraphy of China”, 1989, Beijing: Geological Publishing House

Xu D T, Wang X Q, Shi X Y, . Nitrogen Cycle Perturbations Linked to Metazoan Diversification during the Early Cambrian. Palaeogeography, Palaeoclimatology, Palaeoecology, 2020, 538 109392

Yang D B, Xu W L, Xu Y G, . U−Pb Ages and Hf Isotope Data from Detrital Zircons in the Neoproterozoic Sandstones of Northern Jiangsu and Southern Liaoning Provinces, China: Implications for the Late Precambrian Evolution of the Southeastern North China Craton. Precambrian Research, 2012, 216/217/218/219: 162-176.

Yin C. Micropaleoflora from the Late Precambrian in Huainan Region of Anhui Province and Its Stratigraphic Significance. Professional Papers of Stratigraphy and Palaeontology, Chinese Academy of Geological Sciences, 1985, 12: 97-119. (in Chinese)

Yin L M, Sun W G. Microbiota from the Neoproterozoic Liulaobei Formation in the Huainan Region, Northern Anhui, China. Precambrian Research, 1994, 65(1/2/3/4): 95-114.

Zang W L, Walter M R. Late Proterozoic and Early Cambrian Microfossils and Biostratigraphy, Northern Anhui and Jiangsu, Central-Eastern China. Precambrian Research, 1992, 57(3/4): 243-323.

Zerkle A L, Poulton S W, Newton R J, . Onset of the Aerobic Nitrogen Cycle during the Great Oxidation Event. Nature, 2017, 542: 465-467.

Zhang K, Zhu X, Wood R A, . Oxygenation of the Mesoproterozoic Ocean and the Evolution of Complex Eukaryotes. Nature Geoscience, 2018, 11: 345-350.

Zhang S C, Wang X M, Wang H J, . Sufficient Oxygen for Animal Respiration 1 400 Million Years Ago. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(7): 1731-1736.

Zhang X N, Sigman D M, Morel F M M, . Nitrogen Isotope Fractionation by Alternative Nitrogenases and Past Ocean Anoxia. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(13): 4782-4787.

Zhao H Q, Zhang S H, Ding J K, . New Geochronologic and Paleomagnetic Results from Early Neoproterozoic Mafic Sills and Late Mesoproterozoic to Early Neoproterozoic Successions in the Eastern North China Craton, and Implications for the Reconstruction of Rodinia. GSA Bulletin, 2020, 132(3/4): 739-766.