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Science Journals — AAAS RESEARCH EARLY ANIMALS years. For instance, hopanes are the hydrocarbon remains of bacterial hopanepolyols, whereas sat- urated steranes and aromatic steroids are diage- Ancient steroids establish netic products of eukaryotic sterols. The most common sterols of Eukarya possess a cholester- oid, ergosteroid, or stigmasteroid skeleton with the Ediacaran fossil Dickinsonia 27, 28, or 29 carbon atoms, respectively. These C27 to C29 sterols, distinguished by the alkylation as one of the earliest animals patternatpositionC-24inthesterolsidechain, function as membrane modifiers and are widely 1 1 2 3 distributed across extant Eukarya, but their rela- Ilya Bobrovskiy *, Janet M. Hope , Andrey Ivantsov , Benjamin J. Nettersheim , 3,4 1 tive abundances can give clues about the source Christian Hallmann , Jochen J. Brocks * organisms (24). Apart from Dickinsonia (Fig.1B),whichis The enigmatic Ediacara biota (571 million to 541 million years ago) represents the first one of the most recognizable Ediacaran fossils, macroscopic complex organisms in the geological record and may hold the key to our dickinsoniids include Andiva (Fig. 1C and fig. understanding of the origin of animals. Ediacaran macrofossils are as “strange as life on S1), Vendia, Yorgia, and other flattened Edia- another planet” and have evaded taxonomic classification, with interpretations ranging from caran organisms with segmented metameric marine animals or giant single-celled protists to terrestrial lichens. Here, we show that lipid bodies and a median line along the body axes, biomarkers extracted from organically preserved Ediacaran macrofossils unambiguously separating the “segments.” The specimens for clarify their phylogeny. Dickinsonia and its relatives solely produced cholesteroids, a Downloaded from this study were collected from two surfaces in hallmark of animals. Our results make these iconic members of the Ediacara biota the oldest the Lyamtsa (Dickinsonia)andZimnieGory confirmed macroscopic animals in the rock record, indicating that the appearance of the (Andiva) localities of the Ediacara biota in Ediacara biota was indeed a prelude to the Cambrian explosion of animal life. the White Sea region (Russia). Both Dickinsonia and Andiva are preserved in negative hyporelief he Ediacara biota remains one of the great- nental depositional environment (18), for many on the sole of sandstones with microbial mat est mysteries in paleontology. Members of Ediacaran fossils, including dickinsoniids, it cur- impressions and consist of a thin (up to ~3 mm) http://science.sciencemag.org/ this assemblage were initially described as rently seems impossible to distinguish between film of organic matter. The organic matter was T animals (1, 2); however, as collections grew, giant protist and metazoan origins (4, 19). Some detached from the rock surface (fig. S1) and ex- it became apparent that Ediacaran fossils Ediacaran fossils, such as Palaeopascichnus,were tracted for hydrocarbon biomarkers under strict and their body plans are difficult to compare likely giant unicellular eukaryotes (protists) exclusion of contamination (materials and meth- with modern phyla (3, 4). A major complication (16), which means that in contrast to modern ods). Much thinner organic films covering the for the study of Ediacaran organisms is their soft- ecosystems, these organisms were present and surfaces around Andiva fossils from the Zimnie bodied nature and particular mode of preserva- sometimes extremely abundant in shallow-water Gory locality were extracted as well, providing a tion, rarely found in younger fossils. Thus, the Ediacaran habitats (20). Features of dickinsoniids background signal coming from associated mi- interpretation of various members of the Ediacara such as “quilting” patterns, the inferred absence crobial mats. Investigation of biomarker compo- biota has crossed several Kingdoms and Domains, of dorso-ventral differentiation, and putative ex- sition of surrounding surfaces and enclosing ranging from bacterial colonies (5), marine fungi ternal digestion mode were found to be compat- sedimentary rocks allowed us not only to sub- on September 24, 2018 (6), lichens (7), and giant protists (8, 9)tostem- ible with modern giant protists and hard to tract the background signal but also to make group animals and crown-group Eumetazoa reconcile with metazoans (8, 20). Some modern sure that the biomarker signal from the fossils (4, 10, 11). The recent general consensus is that giant protists can be up to 25 cm in size (21). In is not contaminated (supplementary text). We these fossils are polyphyletic (12, 13): At least the absence of metazoan competition, they may analyzed biomarkers using gas chromatography– some members of the Ediacara biota are almost have become even larger, possibly providing an mass spectrometry (materials and methods). unanimously interpreted as bilaterian animals explanation for the size range of Ediacaran pro- The deposits immediately above and below (Kimberella)(14, 15), whereas others are confident- tistan fossils (8). Some giant protists even have a Dickinsonia are characterized by a monoaromatic ly ascribed to giant protozoa (Palaeopascichnus) motile lifestyle, compatible with Ediacaran trace steroid distribution of 10.6 to 11.9% cholesteroids, (16). Beltanelliformis—although previously inter- fossils (22) and dickinsoniid “footprints” (15). For 13.4 to 16.8% ergosteroids, and 71.3 to 76.0% preted as bacteria, benthic and planktonic algae, dickinsoniids, the absence of evidence for a stigmasteroids, which is consistent with the as well as different animals—is now recognized mouth and gut, perceived absence of bilateral general steroid distribution of sediments at the as a spherical colony of cyanobacteria on the basis symmetry, and possible external digestion are Lyamtsa locality (Fig. 1). The strong stigmaste- of their biomarker content (17). The affinity of all consistent with a protistan origin. However, roid predominance is typical for the Ediacaran most other Ediacarans, however, remains con- all of the above characteristics are also com- period and presumably related to green algae troversial, even at the Kingdom level (4). Most patible with basal Metazoa such as the Placozoa (Chlorophyta) inhabiting benthic mats or the recently, arguments surrounding these fossils that are situated at the very base of Eumetazoa (23), water column (25). In these and all other Edia- have centered on lichens, giant protists, and stem- whereas rejection of an external digestion mode caran sediment samples from the White Sea re- or crown-group Metazoa. and acceptance of supposed cephalization (15)may gion, the carbon-number distribution of saturated Whereas the lichen hypothesis (7) requires place dickinsoniids even higher on the metazoan steranes is nearly identical to the distribution an implausible reinterpretation of the habitat of tree. The nature of dickinsoniids, and most other of monoaromatic steroid homologs and always the Ediacara biota from a marine to a conti- Ediacaran fossils, thus remains unresolved. dominated by green algal stigmasteroids (Table 1). We applied a new approach (17) to test the By contrast, biomarkers extracted from the iso- lichen, protist, and animal hypotheses by study- lated organic matter of the largest Dickinsonia 1Research School of Earth Sciences, Australian National University, Canberra ACT 2601, Australia. 2Borissiak ing biomarkers extracted from organically pre- specimen had a monoaromatic steroid distribu- Paleontological Institute, Russian Academy of Sciences, Moscow served dickinsoniids. Hydrocarbon biomarkers tion of 93% cholesteroids, 1.8% ergosteroids, and 117997, Russia. 3Max Planck Institute for Biogeochemistry, Jena are the molecular fossils of lipids and other bio- 5.2% stigmasteroids (Fig. 1A and Table 1). A gen- 4 – 07745, Germany. MARUM Center for Marine Environmental logical compounds. Encased in sedimentary rock, eral trend of increasing monoaromatic choles- Sciences, University of Bremen, Bremen 28359, Germany. *Corresponding author. Email: [email protected] biomarkers may retain information about their teroid abundance from 84.8 to 93.0% from the (I.B.); [email protected] (J.J.B.) biological origins for hundreds of millions of smaller to the larger Dickinsonia specimens Bobrovskiy et al., Science 361, 1246–1249 (2018) 21 September 2018 1of4 RESEARCH | REPORT Fig. 1. Biomarkers from organi- A I+V Dickinsonia cally preserved . D (A) Mass/charge ratio 253 selected 16 cholesteroids C27 ion recording chromatogram 14 I Dickinsonia showing the distribution of 12 ergosteroids C28 10 Andiva monoaromatic steroids (MAS) 27 29 8 of the solvent extract of a large Bulk extracts stigmasteroids C29 6 Dickinsonia specimen (Dickinsonia- CAS /C Dickinsonia size M 4 0 1 2 3 4 5 6 2; 5.5 cm width). (B) Organically 2 Dickinsonia cm preserved from the 0 Lyamtsa locality (Dickinsonia-2). 035810 (C) Metastable reaction monitoring ADI chromatogram showing the sum II+VII II V VII of C27–29 sterane traces of I+V Dickinsonia-2. abb =5a(H), 14b(H), I+V VII VII VIIII I+V VII II 17b(H) (and correspondingly for aaa and baa); S and R indicate 60.00 60.50 61.00 61.50 62.00 62.50 63.00 63.50 64.00 63.50 64.00 64.50 min isomerization at position C-20. (D) Relationship between the B C MAS C /MAS C ratio and the Downloaded from 27 29 E 6 Animal Decomposition Index b a b a 5 (ADI) = (C27 5 /5 )/(C29 5 /5 )in Dickinsonia Dickinsonia (n = 6 samples), Andiva 4 27 Andiva n ( = 2 samples), and bulk rock C βαα R α 3 Bulk extracts extracts from the Lyamtsa and /5 + β 2 Zimnie Gory localities (n = αααS 5 Dickinsonia size 0 1 2 3 4 5 6 http://science.sciencemag.org/ 32 samples). Only samples with 1 2 R = 0.83 cm detectable MAS were used in the 0 plot. ADI is a measure of the 0.0 0.5 1.0 1.5 2.0 β α quantity of sterols that 5 /5 C29 decomposed in the anaerobic microenvironment of an animal carcass relative to normal sterol βααR αααR decomposition within the + ≈ αββ background sediment. ADI 1 βααS αααR R indicates that cholesteroids αββ βαα βαα and stigmasteroids underwent R S ααα αββ S S ααα on September 24, 2018 alteration in the same diagenetic S αααR environment consistent with the absence of animal tissue.
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