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      Decimetre-scale multicellular eukaryotes from the 1.56-billion-year-old Gaoyuzhuang Formation in North China

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          Abstract

          Fossils of macroscopic eukaryotes are rarely older than the Ediacaran Period (635–541 million years (Myr)), and their interpretation remains controversial. Here, we report the discovery of macroscopic fossils from the 1,560-Myr-old Gaoyuzhuang Formation, Yanshan area, North China, that exhibit both large size and regular morphology. Preserved as carbonaceous compressions, the Gaoyuzhuang fossils have statistically regular linear to lanceolate shapes up to 30 cm long and nearly 8 cm wide, suggesting that the Gaoyuzhuang fossils record benthic multicellular eukaryotes of unprecedentedly large size. Syngenetic fragments showing closely packed ∼10 μm cells arranged in a thick sheet further reinforce the interpretation. Comparisons with living thalloid organisms suggest that these organisms were photosynthetic, although their phylogenetic placement within the Eukarya remains uncertain. The new fossils provide the strongest evidence yet that multicellular eukaryotes with decimetric dimensions and a regular developmental program populated the marine biosphere at least a billion years before the Cambrian Explosion.

          Abstract

          Macroscopic organisms are rare in the fossil record until the Ediacaran Period, beginning 635 million years ago. Here, Zhu et al. report the discovery of 1.56-billion-year-old carbonaceous compression fossils that provide evidence of the evolution of macroscopic, multicellular eukaryotes long before the Ediacaran Period.

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          Most cited references11

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          Estimating the timing of early eukaryotic diversification with multigene molecular clocks.

          Although macroscopic plants, animals, and fungi are the most familiar eukaryotes, the bulk of eukaryotic diversity is microbial. Elucidating the timing of diversification among the more than 70 lineages is key to understanding the evolution of eukaryotes. Here, we use taxon-rich multigene data combined with diverse fossils and a relaxed molecular clock framework to estimate the timing of the last common ancestor of extant eukaryotes and the divergence of major clades. Overall, these analyses suggest that the last common ancestor lived between 1866 and 1679 Ma, consistent with the earliest microfossils interpreted with confidence as eukaryotic. During this interval, the Earth's surface differed markedly from today; for example, the oceans were incompletely ventilated, with ferruginous and, after about 1800 Ma, sulfidic water masses commonly lying beneath moderately oxygenated surface waters. Our time estimates also indicate that the major clades of eukaryotes diverged before 1000 Ma, with most or all probably diverging before 1200 Ma. Fossils, however, suggest that diversity within major extant clades expanded later, beginning about 800 Ma, when the oceans began their transition to a more modern chemical state. In combination, paleontological and molecular approaches indicate that long stems preceded diversification in the major eukaryotic lineages.
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            A molecular timeline for the origin of photosynthetic eukaryotes.

            The appearance of photosynthetic eukaryotes (algae and plants) dramatically altered the Earth's ecosystem, making possible all vertebrate life on land, including humans. Dating algal origin is, however, frustrated by a meager fossil record. We generated a plastid multi-gene phylogeny with Bayesian inference and then used maximum likelihood molecular clock methods to estimate algal divergence times. The plastid tree was used as a surrogate for algal host evolution because of recent phylogenetic evidence supporting the vertical ancestry of the plastid in the red, green, and glaucophyte algae. Nodes in the plastid tree were constrained with six reliable fossil dates and a maximum age of 3,500 MYA based on the earliest known eubacterial fossil. Our analyses support an ancient (late Paleoproterozoic) origin of photosynthetic eukaryotes with the primary endosymbiosis that gave rise to the first alga having occurred after the split of the Plantae (i.e., red, green, and glaucophyte algae plus land plants) from the opisthokonts sometime before 1,558 MYA. The split of the red and green algae is calculated to have occurred about 1,500 MYA, and the putative single red algal secondary endosymbiosis that gave rise to the plastid in the cryptophyte, haptophyte, and stramenopile algae (chromists) occurred about 1,300 MYA. These dates, which are consistent with fossil evidence for putative marine algae (i.e., acritarchs) from the early Mesoproterozoic (1,500 MYA) and with a major eukaryotic diversification in the very late Mesoproterozoic and Neoproterozoic, provide a molecular timeline for understanding algal evolution.
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              Eukaryotic organisms in Proterozoic oceans.

              The geological record of protists begins well before the Ediacaran and Cambrian diversification of animals, but the antiquity of that history, its reliability as a chronicle of evolution and the causal inferences that can be drawn from it remain subjects of debate. Well-preserved protists are known from a relatively small number of Proterozoic formations, but taphonomic considerations suggest that they capture at least broad aspects of early eukaryotic evolution. A modest diversity of problematic, possibly stem group protists occurs in ca 1800-1300 Myr old rocks. 1300-720 Myr fossils document the divergence of major eukaryotic clades, but only with the Ediacaran-Cambrian radiation of animals did diversity increase within most clades with fossilizable members. While taxonomic placement of many Proterozoic eukaryotes may be arguable, the presence of characters used for that placement is not. Focus on character evolution permits inferences about the innovations in cell biology and development that underpin the taxonomic and morphological diversification of eukaryotic organisms.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                17 May 2016
                2016
                : 7
                : 11500
                Affiliations
                [1 ]Tianjin Institute of Geology and Mineral Resources, China Geological Survey , Tianjin 300170, China
                [2 ]State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences , Wuhan 430074, China
                [3 ]State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences , Nanjing 210008, China
                [4 ]Department of Organismic and Evolutionary Biology, Harvard University , Cambridge, Massachusetts 02138, USA
                [5 ]Centre for Geobiology, University of Bergen , Bergen 5007, Norway
                Author notes
                Article
                ncomms11500
                10.1038/ncomms11500
                4873660
                27186667
                71e1d92a-360c-4c62-8553-b05f0a3187a1
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 21 November 2015
                : 04 April 2016
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