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Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era

Abstract

The Neoproterozoic era (about 1,000 to 542 million years ago) was a time of turbulent environmental change. Large fluctuations in the carbon cycle were associated with at least two severe — possible Snowball Earth — glaciations. There were also massive changes in the redox state of the oceans, culminating in the oxygenation of much of the deep oceans. Amid this environmental change, increasingly complex life forms evolved. The traditional view is that a rise in atmospheric oxygen concentrations led to the oxygenation of the ocean, thus triggering the evolution of animals. We argue instead that the evolution of increasingly complex eukaryotes, including the first animals, could have oxygenated the ocean without requiring an increase in atmospheric oxygen. We propose that large eukaryotic particles sank quickly through the water column and reduced the consumption of oxygen in the surface waters. Combined with the advent of benthic filter feeding, this shifted oxygen demand away from the surface to greater depths and into sediments, allowing oxygen to reach deeper waters. The decline in bottom-water anoxia would hinder the release of phosphorus from sediments, potentially triggering a potent positive feedback: phosphorus removal from the ocean reduced global productivity and ocean-wide oxygen demand, resulting in oxygenation of the deep ocean. That, in turn, would have further reinforced eukaryote evolution, phosphorus removal and ocean oxygenation.

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Figure 1: Timeline of biological and environmental changes spanning the Cryogenian, Ediacaran and Cambrian periods.
Figure 2: Key steps and feedbacks in the co-evolution of eukaryotes and ocean redox state.

References

  1. 1

    Lenton, T. M. & Watson, A. J. Revolutions that made the Earth. (Oxford Univ. Press, 2011).

    Book  Google Scholar 

  2. 2

    Butterfield, N. J. Animals and the invention of the Phanerozoic Earth system. Trends Ecol. Evol. 26, 81–87 (2011).

    Article  Google Scholar 

  3. 3

    Knoll, A. H., The multiple origins of complex multicellularity. Annu. Rev. Earth Planet. Sci. 39, 217–239 (2011).

    Article  Google Scholar 

  4. 4

    Canfield, D. E., Poulton, S. W. & Narbonne, G. M. Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92–95 (2007).

    Article  Google Scholar 

  5. 5

    Sahoo, S. K. et al., Ocean oxygenation in the wake of the Marinoan glaciation. Nature 489, 546–549 (2012).

    Article  Google Scholar 

  6. 6

    Nursall, J. R. Oxygen as a prerequisite to the origin of the Metazoa. Nature 183, 1170–1172 (1959).

    Article  Google Scholar 

  7. 7

    Raff, R. A. & Raff, E. C. Respiratory mechanisms and the metazoan fossil record. Nature 228, 1003–1005 (1970).

    Article  Google Scholar 

  8. 8

    Towe, K. M., Oxygen-collagen priority and the Early Metazoan fossil record. Proc. Natl Acad. Sci. USA 65, 781–788 (1970).

    Article  Google Scholar 

  9. 9

    Catling, D. C., Glein, C. G., Zahnle, K. J. & McKay, C. P. Why O2 is required by complex life on habitable planets and the concept of planetary “oxygenation time”. Astrobiology 5, 415–438 (2005).

    Article  Google Scholar 

  10. 10

    Budd, G. E. The earliest fossil record of the animals and its significance. Phil. Trans. R. Soc. B: Biol. Sci. 363, 1425–1434 (2008).

    Article  Google Scholar 

  11. 11

    Sperling, E. A., Halverson, G. P., Knoll, A. H., Macdonald, F. A. & Johnston, D. T. A basin redox transect at the dawn of animal life. Earth Planet. Sci. Lett. 371–372, 143–155 (2013).

  12. 12

    Poulton, S. W. & Canfield, D. E. Ferruginous conditions: a dominant feature of the ocean through Earth's history. Elements 7, 107–112 (2011).

    Article  Google Scholar 

  13. 13

    Kasting, J. F. Box models for the evolution of atmospheric oxygen: an update. Glob. Planet. Change 97, 125–131 (1991).

    Article  Google Scholar 

  14. 14

    Kendall, B. et al. Pervasive oxygenation along late Archaean ocean margins. Nature Geosci 3, 647–652 (2010).

    Article  Google Scholar 

  15. 15

    Slack, J. F., Grenne, T., Bekker, A., Rouxel, O. J. & Lindberg, P. A. Suboxic deep seawater in the late Paleoproterozoic: evidence from hematitic chert and iron formation related to seafloor-hydrothermal sulfide deposits, central Arizona, USA. Earth Planet. Sci. Lett. 255, 243–256 (2007).

    Article  Google Scholar 

  16. 16

    Canfield, D. E. et al. Ferruginous conditions dominated later Neoproterozoic deep-water chemistry. Science 321, 949–952 (2008).

    Article  Google Scholar 

  17. 17

    Frei, R., Gaucher, C., Poulton, S. W. & Canfield, D. E. Fluctuations in Precambrian atmospheric oxygenation recorded by chromium isotopes. Nature 461, 250–253 (2009).

    Article  Google Scholar 

  18. 18

    Partin, C. A. et al. Large-scale fluctuations in Precambrian atmospheric and oceanic oxygen levels from the record of U in shales. Earth Planet. Sci. Lett. 369–370, 284–293 (2013).

    Article  Google Scholar 

  19. 19

    Logan, G. B., Hayes, J. M., Hieshima, G. B. & Summons, R. E. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376, 53–56 (1995).

    Article  Google Scholar 

  20. 20

    Parfrey, L. W., Lahr, D. J. G., Knoll, A. H. & Katz, L. A. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl Acad. Sci. USA 108, 13624–13629 (2011).

    Article  Google Scholar 

  21. 21

    Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

    Article  Google Scholar 

  22. 22

    Butterfield, N. J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386–404 (2000).

    Article  Google Scholar 

  23. 23

    Strother, P. K., Battison, L., Brasier, M. D. & Wellman, C. H. Earth's earliest non-marine eukaryotes. Nature 473, 505–509 (2011).

    Article  Google Scholar 

  24. 24

    Pawlowska, M. M., Butterfield, N. J. & Brocks, J. J. Lipid taphonomy in the Proterozoic and the effect of microbial mats on biomarker preservation. Geology 41, 103–106 (2013).

    Article  Google Scholar 

  25. 25

    Canfield, D. E., The early history of atmospheric oxygen: homage to Robert M. Garrels. Annu. Rev. Earth Planet. Sci. 33, 1–36 (2005).

    Article  Google Scholar 

  26. 26

    Rye, R. & Holland, H. D. Paleosols and the evolution of atmospheric oxygen: a critical review. Am. J. Sci. 298, 621–672 (1998).

    Article  Google Scholar 

  27. 27

    Planavsky, N. J. et al. Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477, 448–451 (2011).

    Article  Google Scholar 

  28. 28

    Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008).

    Article  Google Scholar 

  29. 29

    Reinhard, C. T. et al. Proterozoic ocean redox and biogeochemical stasis. Proc. Natl Acad. Sci. USA 110, 5357–5362 (2013).

    Article  Google Scholar 

  30. 30

    Kendall, B., Gordon, G. W., Poulton, S. W. & Anbar, A. D. Molybdenum isotope constraints on the extent of late Paleoproterozoic ocean euxinia. Earth Planet. Sci. Lett. 307, 450–460 (2011).

    Article  Google Scholar 

  31. 31

    Poulton, S. W., Fralick, P. W. & Canfield, D. E. Spatial variability in oceanic redox structure 1.8 billion years ago. Nature Geosci. 3, 486–490 (2010).

    Article  Google Scholar 

  32. 32

    Ozaki, K. & Tajika, E. Biogeochemical effects of atmospheric oxygen concentration, phosphorus weathering, and sea-level stand on oceanic redox chemistry: implications for greenhouse climates. Earth Planet. Sci. Lett. 373, 129–139 (2013).

    Article  Google Scholar 

  33. 33

    Canfield, D. E. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998).

    Article  Google Scholar 

  34. 34

    Planavsky, N. J. et al. The evolution of the marine phosphate reservoir. Nature 467, 1088–1090 (2010).

    Article  Google Scholar 

  35. 35

    Boyle, R. A. et al. Nitrogen cycle feedbacks as a control on euxinia in the mid-Proterozoic ocean. Nature Commun. 4, 1533 (2013).

    Article  Google Scholar 

  36. 36

    Godfrey, L. V., Poulton, S. W., Bebout, G. E. & Fralick, P. W. Stability of the nitrogen cycle during development of sulfidic water in the redox-stratified late Paleoproterozoic Ocean. Geology 41, 655–658 (2013).

    Article  Google Scholar 

  37. 37

    Kah, L. C., Lyons, T. W. & Frank, T. D. Low marine sulphate and protracted oxygenation of the Proterozoic biosphere. Nature 431, 834–838 (2004).

    Article  Google Scholar 

  38. 38

    Ingall, E. & Jahnke, R. Evidence for enhanced phosphorus regeneration from marine sediments overlain by oxygen depleted waters. Geochim. Cosmochim. Acta 58, 2571–2575 (1994).

    Article  Google Scholar 

  39. 39

    Colman, A. S. & Holland, H. D. in Marine Authigenesis: from Global to Microbial Vol. 65 (eds Glenn, C. R., Lucas, J. & Prévôt-Lucas, L.) 53–75 (SEPM, 2000).

    Book  Google Scholar 

  40. 40

    Van Cappellen, P. & Ingall, E. D. Benthic phosphorus regeneration, net primary production, and ocean anoxia: a model of the coupled marine biogeochemical cycles of carbon and phosphorus. Paleoceanography 9, 677–692 (1994).

    Article  Google Scholar 

  41. 41

    Handoh, I. C. & Lenton, T. M. Periodic mid-Cretaceous Oceanic Anoxic Events linked by oscillations of the phosphorus and oxygen biogeochemical cycles. Glob. Biogeochem. Cycles 17, 1092 (2003).

    Article  Google Scholar 

  42. 42

    Javaux, E. in Origins and Evolution of Life: An Astrobiological Perspective (eds Gargaud, M., Lopez-Garcia, P. & Martin, H.) 414–449 (Cambridge Univ. Press, 2011).

    Google Scholar 

  43. 43

    Porter, S. M. & Knoll, A. H. Testate amoebae in the Neoproterozoic Era: evidence from vase-shaped microfossils in the Chuar Group, Grand Canyon. Paleobiology 26, 360–385 (2000).

    Article  Google Scholar 

  44. 44

    Summons, R. E. et al. Distinctive hydrocarbon biomarkers from fossiliferous sediment of the Late Proterozoic Walcott Member, Chuar Group, Grand Canyon, Arizona. Geochimica et Cosmochimica Acta 52, 2625–2637 (1988).

    Article  Google Scholar 

  45. 45

    Cohen, P. A., Schopf, J. W., Butterfield, N. J., Kudryavtsev, A. B. & Macdonald, F. A., Phosphate biomineralization in mid-Neoproterozoic protists. Geology 39, 539–542 (2011).

    Article  Google Scholar 

  46. 46

    Lebrato, M. et al., Jelly biomass sinking speed reveals a fast carbon export mechanism. Limnology and Oceanography 58, 1113–1122 (2013).

    Article  Google Scholar 

  47. 47

    Butterfield, N. J. Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7 (2009).

    Article  Google Scholar 

  48. 48

    Tziperman, E., Halevy, I., Johnston, D. T., Knoll, A. H. & Schrag, D. P. Biologically induced initiation of Neoproterozoic snowball-Earth events. Proc. Natl Acad. Sci. USA 108, 15091–15096 (2011).

    Article  Google Scholar 

  49. 49

    Johnston, D. T. et al. An emerging picture of Neoproterozoic ocean chemistry: Insights from the Chuar Group, Grand Canyon, USA. Earth Planet. Sci. Letters 290, 64–73 (2010).

    Article  Google Scholar 

  50. 50

    Och, L. M. & Shields-Zhou, G. A. The Neoproterozoic oxygenation event: Environmental perturbations and biogeochemical cycling. Earth-Sci. Rev. 110, 26–57 (2012).

    Article  Google Scholar 

  51. 51

    Derry, L. A., Kaufman, A. J. & Jacobsen, S. B., Sedimentary cycling and environmental change in the Late Proterozoic: Evidence from stable and radiogenic isotopes. Geochim. Cosmochim. Acta 56, 1317–1329 (1992).

    Article  Google Scholar 

  52. 52

    Carver, J. H. & Vardavas, I. M., Precambrian glaciations and the evolution of the atmosphere. Ann. Geophys. 12, 674–682 (1994).

    Article  Google Scholar 

  53. 53

    Lenton, T. M. & Watson, A. J. Biotic enhancement of weathering, atmospheric oxygen and carbon dioxide in the Neoproterozoic. Geophys. Res. Lett. 31, L05202 (2004).

    Article  Google Scholar 

  54. 54

    Donnadieu, Y., Godderis, Y., Ramstein, G., Nedelec, A. & Meert, J. A 'snowball Earth' climate triggered by continental break-up through changes in runoff. Nature 428, 303–306 (2004).

    Article  Google Scholar 

  55. 55

    Li, Z. X. et al. Geochronology of Neoproterozoic syn-rift magmatism in the Yangtze Craton, South China and correlations with other continents: evidence for a mantle superplume that broke up Rodinia. Precambr. Res. 122, 85–109 (2003).

    Article  Google Scholar 

  56. 56

    Macdonald, F. A. et al. Calibrating the Cryogenian. Science 327, 1241–1243 (2010).

    Article  Google Scholar 

  57. 57

    Shields-Zhou, G. A. & Och, L. M. The case for a Neoproterozoic Oxygenation Event: Geochemical evidence and biological consequences. GSA Today 21, 4–11 (2011).

    Article  Google Scholar 

  58. 58

    Dahl, T. W. et al. Molybdenum evidence for expansive sulfidic water masses in 750 Ma oceans. Earth Planet. Sci. Lett. 311, 264–274 (2011).

    Article  Google Scholar 

  59. 59

    Nagy, R. M., Porter, S. M., Dehler, C. M. & Shen, Y. Biotic turnover driven by eutrophication before the Sturtian low-latitude glaciation. Nature Geosci. 2, 415–418 (2009).

    Article  Google Scholar 

  60. 60

    Vincent, W. F. et al. Ice shelf microbial ecosystems in the high Arctic and implications for life on Snowball Earth. Naturwissenschaften 87, 137–141 (2000).

    Article  Google Scholar 

  61. 61

    Knoll, A. H., Javaux, E. J., Hewitt, D. & Cohen, P. Eukaryotic organisms in Proterozoic oceans. Phil. Trans. R. Soc. B: Biol. Sci. 361, 1023–1038 (2006).

    Article  Google Scholar 

  62. 62

    Maloof, A. C. et al. Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nature Geosci 3, 653–659 (2010).

    Article  Google Scholar 

  63. 63

    Love, G. D. et al. Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature 457, 718–721 (2009).

    Article  Google Scholar 

  64. 64

    Antcliffe, J. B. Questioning the evidence of organic compounds called sponge biomarkers. Palaeontology 56, 917–925 (2013).

    Google Scholar 

  65. 65

    Vogel, S. Current-induced flow through living sponges in nature. Proc. Natl Acad. Sci. USA 74, 2069–2071 (1977).

    Article  Google Scholar 

  66. 66

    Erwin, D. & Tweedt, S. Ecological drivers of the Ediacaran-Cambrian diversification of Metazoa. Evol. Ecol. 26, 417–433 (2012).

    Article  Google Scholar 

  67. 67

    Reiswig, H. M. Water transport, respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol. 14, 231–249 (1974).

    Article  Google Scholar 

  68. 68

    Perea-Blazquez, A., Davy, S. K. & Bell, J. J. Estimates of particulate organic carbon flowing from the pelagic environment to the benthos through sponge assemblages. PLoS ONE 7, e29569 (2012).

    Article  Google Scholar 

  69. 69

    De Goeij, J., van den Berg, H., van Oostveen, M., Epping, E. & van Duyl, F. Major bulk dissolved organic carbon (DOC) removal by encrusting coral reef cavity sponges. Marine Ecol. Progress Series 357, 139–151 (2008).

    Article  Google Scholar 

  70. 70

    Cook, P. J. & Shergold, J. H. eds. Phosphate deposits of the world: Volume 1, Proterozoic and Cambrian phosphorites. (Cambridge Univ. Press, 2005).

    Google Scholar 

  71. 71

    Shen, Y., Zhang, T. & Hoffman, P. F. On the coevolution of Ediacaran oceans and animals. Proc. Natl Acad. Sci. USA 105, 7376–7381 (2008).

    Article  Google Scholar 

  72. 72

    Li, C. et al., A stratified redox model for the Ediacaran Ocean. Science 328, 80–83 (2010).

    Article  Google Scholar 

  73. 73

    Mills, B., Watson, A. J., Goldblatt, C., Boyle, R. & Lenton, T. M. Timing of Neoproterozoic glaciations linked to transport-limited global weathering. Nature Geosci. 4, 861–864 (2011).

    Article  Google Scholar 

  74. 74

    Yuan, X., Chen, Z., Xiao, S., Zhou, C. & Hua, H. An early Ediacaran assemblage of macroscopic and morphologically differentiated eukaryotes. Nature 470, 390–393 (2011).

    Article  Google Scholar 

  75. 75

    Kremien, M., Shavit, U., Mass, T. & Genin, A. Benefit of pulsation in soft corals. Proc. Natl Acad. Sci. USA 110, 8978–8983 (2013).

    Article  Google Scholar 

  76. 76

    Jantzen, C., Wild, C., Rasheed, M., El-Zibdah, M. & Richter, C. Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef. Marine Ecol. Progress Series 411, 117–125 (2010).

    Article  Google Scholar 

  77. 77

    Sperling, E. A. et al. Oxygen, ecology, and the Cambrian radiation of animals. Proc. Natl Acad. Sci. USA 110, 13446–13451 (2013).

    Article  Google Scholar 

  78. 78

    Condon, D. et al. U-Pb Ages from the Neoproterozoic Doushantuo Formation, China. Science 308, 95–98 (2005).

    Article  Google Scholar 

  79. 79

    Rothman, D. H., Hayes, J. M. & Summons, R. E. Dynamics of the Neoproterozoic carbon cycle. Proc. Natl Acad. Sci. USA 100, 8124–8129 (2003).

    Article  Google Scholar 

  80. 80

    Bristow, T. F. & Kennedy, M. J. Carbon isotope excursions and the oxidant budget of the Ediacaran atmosphere and ocean. Geology 36, 863–866 (2008).

    Article  Google Scholar 

  81. 81

    Derry, L. A. A burial diagenesis origin for the Ediacaran Shuram-Wonoka carbon isotope anomaly. Earth Planet. Sci. Letters 294, 152–162 (2010).

    Article  Google Scholar 

  82. 82

    Grotzinger, J. P., Fike, D. A. & Fischer, W. W. Enigmatic origin of the largest-known carbon isotope excursion in Earth's history. Nature Geosci. 4, 285–292 (2011).

    Article  Google Scholar 

  83. 83

    Knauth, L. P. & Kennedy, M. J. The late Precambrian greening of the Earth. Nature 460, 728–732 (2009).

    Article  Google Scholar 

  84. 84

    Lu, M. et al. The DOUNCE event at the top of the Ediacaran Doushantuo Formation, South China: Broad stratigraphic occurrence and non-diagenetic origin. Precambr. Res. 225, 86–109 (2013).

    Article  Google Scholar 

  85. 85

    Bjerrum, C. J. & Canfield, D. E. Towards a quantitative understanding of the late Neoproterozoic carbon cycle. Proc. Natl Acad. Sci. USA 108, 5542–5547 (2011).

    Article  Google Scholar 

  86. 86

    Liu, A. G., Mcllroy, D. & Brasier, M. D. First evidence for locomotion in the Ediacara biota from the 565 Ma Mistaken Point Formation, Newfoundland. Geology 38, 123–126 (2010).

    Article  Google Scholar 

  87. 87

    Martin, M. W. et al. Age of Neoproterozoic bilatarian body and trace fossils, White Sea, Russia: implications for Metazoan evolution. Science 288, 841–845 (2000).

    Article  Google Scholar 

  88. 88

    Jensen, S., Saylor, B. Z., Gehling, J. G. & Germs, G. J. B. Complex trace fossils from the terminal Proterozoic of Namibia. Geology 28, 143–146 (2000).

    Article  Google Scholar 

  89. 89

    Canfield, D. E. & Farquhar, J. Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proc. Natl Acad. Sci. USA 106, 8123–8127 (2009).

    Article  Google Scholar 

  90. 90

    Zhang, L. et al. Impact of different benthic animals on phosphorus dynamics across the sediment-water interface. J. Environ. Sci. 22, 1674–1682 (2010).

    Article  Google Scholar 

  91. 91

    Sarmiento, J. L., Herbert, T. D. & Toggweiler, J. R. Causes of anoxia in the world ocean. Glob. Biogeochem. Cycles 2, 115–128 (1988).

    Article  Google Scholar 

  92. 92

    Knox, F. & McElroy, M. B. Changes in atmospheric CO2: influence of the marine biota at high latitude. J. Geophys. Res. 89, 4629–4637 (1984).

    Article  Google Scholar 

  93. 93

    Blackstone, N. W. & Ellison, A. M. Maximal indirect development, set-aside cells, and levels of selection. J. Exp. Zool. 288, 99–104 (2000).

    Article  Google Scholar 

  94. 94

    Cameron, R. A., Peterson, K. J. & Davidson, E. H., Developmental gene regulation and the evolution of large animal body plans. Am. Zool. 38, 609–620 (1998).

    Article  Google Scholar 

  95. 95

    Michod, R. E. Darwinian Dynamics. (Princeton, 1999).

    Google Scholar 

  96. 96

    Nichols, S. A., Dirks, W., Pearse, J. S. & King, N., Early evolution of animal cell signaling and adhesion genes. Proc. Natl Acad. Sci. USA 103, 12451–12456 (2006).

    Article  Google Scholar 

  97. 97

    Hamilton, W. D. The evolution of altruistic behavior. Am. Natural. 97, 354–356 (1963).

    Article  Google Scholar 

  98. 98

    Boyle, R. A., Lenton, T. M. & Williams, H. T. P. Neoproterozoic 'snowball Earth' glaciations and the evolution of altruism. Geobiology 5, 337–349 (2007).

    Article  Google Scholar 

  99. 99

    Cohen, D. & Eshel, I. On the founder effect and the evolution of altruistic traits. Theoret. Popul. Biol. 10, 276–302 (1976).

    Article  Google Scholar 

  100. 100

    Brockhurst, M. A. Population bottlenecks promote cooperation in bacterial biofilms. PLoS ONE 2, e634 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the NERC project 'Re-inventing the planet: the Neoproterozoic revolution in oxygenation, biogeochemistry and biological complexity' (NE/I005978/1). We thank Susannah Porter for providing helpful comments.

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T.M.L. wrote the paper with input from all co-authors.

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Correspondence to Timothy M. Lenton.

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Lenton, T., Boyle, R., Poulton, S. et al. Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nature Geosci 7, 257–265 (2014). https://doi.org/10.1038/ngeo2108

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