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Eukaryotic life appears to have flourished surprisingly late in the history of our planet. This view is based on the low diversity of diagnostic eukaryotic fossils in marine sediments of mid-Proterozoic age (around 1,600 to 800 million years ago) and an absence of steranes, the molecular fossils of eukaryotic membrane sterols 1 , 2 . This scarcity of eukaryotic remains is difficult to reconcile with molecular clocks that suggest that the last eukaryotic common ancestor (LECA) had already emerged between around 1,200 and more than 1,800 million years ago. LECA, in turn, must have been preceded by stem-group eukaryotic forms by several hundred million years 3 . Here we report the discovery of abundant protosteroids in sedimentary rocks of mid-Proterozoic age. These primordial compounds had previously remained unnoticed because their structures represent early intermediates of the modern sterol biosynthetic pathway, as predicted by Konrad Bloch 4 . The protosteroids reveal an ecologically prominent ‘protosterol biota’ that was widespread and abundant in aquatic environments from at least 1,640 to around 800 million years ago and that probably comprised ancient protosterol-producing bacteria and deep-branching stem-group eukaryotes. Modern eukaryotes started to appear in the Tonian period (1,000 to 720 million years ago), fuelled by the proliferation of red algae (rhodophytes) by around 800 million years ago. This ‘Tonian transformation’ emerges as one of the most profound ecological turning points in the Earth’s history. Analysis of sedimentary rocks from the mid-Proterozoic interval reveals traces of protosteroids, suggesting the widespread presence of stem-group eukaryotes that predated and co-existed with the crown-group ancestors of modern eukaryotes.

Significance The advent of oxygenic photosynthesis set the stage for the evolution of complex life on an oxygenated planet, but it is unknown when this transformative biochemistry emerged. The existing hydrocarbon biomarker record requires that oxygenic photosynthesis and eukaryotes emerged more than 300 million years before the Great Oxidation Event [∼2.4 billion years ago (Ga)]. We report that hopane and sterane concentrations measured in new ultraclean Archean drill cores from Australia are comparable to blank concentrations, yet their concentrations in the exteriors of conventionally collected cores of stratigraphic equivalence exceed blank concentrations by more than an order of magnitude due to surficial contamination. Consequently, previous hydrocarbon biomarker reports no longer provide valid evidence for the advent of oxygenic photosynthesis and eukaryotes by ∼2.7 Ga. Hopanes and steranes found in Archean rocks have been presented as key evidence supporting the early rise of oxygenic photosynthesis and eukaryotes, but the syngeneity of these hydrocarbon biomarkers is controversial. To resolve this debate, we performed a multilaboratory study of new cores from the Pilbara Craton, Australia, that were drilled and sampled using unprecedented hydrocarbon-clean protocols. Hopanes and steranes in rock extracts and hydropyrolysates from these new cores were typically at or below our femtogram detection limit, but when they were detectable, they had total hopane (<37.9 pg per gram of rock) and total sterane (<32.9 pg per gram of rock) concentrations comparable to those measured in blanks and negative control samples. In contrast, hopanes and steranes measured in the exteriors of conventionally drilled and curated rocks of stratigraphic equivalence reach concentrations of 389.5 pg per gram of rock and 1,039 pg per gram of rock, respectively. Polycyclic aromatic hydrocarbons and diamondoids, which exceed blank concentrations, exhibit individual concentrations up to 80 ng per gram of rock in rock extracts and up to 1,000 ng per gram of rock in hydropyrolysates from the ultraclean cores. These results demonstrate that previously studied Archean samples host mixtures of biomarker contaminants and indigenous overmature hydrocarbons. Therefore, existing lipid biomarker evidence cannot be invoked to support the emergence of oxygenic photosynthesis and eukaryotes by ∼2.7 billion years ago. Although suitable Proterozoic rocks exist, no currently known Archean strata lie within the appropriate thermal maturity window for syngenetic hydrocarbon biomarker preservation, so future exploration for Archean biomarkers should screen for rocks with milder thermal histories.

The Ediacara biota represents the first complex macroscopic organisms in the geological record, foreshadowing the radiation of eumetazoan animals in the Cambrian explosion. However, little is known about the contingencies that lead to their emergence, including the possible roles of nutrient availability and the quality of food sources. Here we present information on primary producers in the Ediacaran based on biomarker molecules that were extracted from sediments hosting Ediacaran macrofossils. High relative abundances of algal steranes over bacterial hopanes suggest that the Ediacara biota inhabited nutrient replete environments with an abundance of algal food sources comparable to Phanerozoic ecosystems. Thus, organisms of the Ediacara biota inhabited nutrient-rich environments akin to those that later fuelled the Cambrian explosion. Complex macroscopic organisms are first found in the Ediacaran period, but their ecology during this time is not well understood. Here, Bobrovskiy et al. analyse biomarkers from Ediacaran sediments hosting macrofossils and find evidence for abundant algal food sources available for these organisms.

The first complex organisms emerged during the Ediacaran period, around 600 million years ago. The taxonomic affiliation of many of these organisms has been difficult to discern. Fossils of Dickinsonia , bilaterally symmetrical oval organisms, have been particularly difficult to classify. Bobrovskiy et al. conducted an analysis using lipid biomarkers obtained from Dickinsonia fossils and found that the fossils contained almost exclusively cholesteroids, a marker found only in animals (see the Perspective by Summons and Erwin). Thus, Dickinsonia were basal animals. This supports the idea that the Ediacaran biota may have been a precursor to the explosion of animal forms later observed in the Cambrian, about 500 million years ago. Science , this issue p. 1246 ; see also p. 1198 Lipid biomarkers extracted from organically preserved Ediacaran macrofossils unambiguously clarify their phylogeny. The enigmatic Ediacara biota (571 million to 541 million years ago) represents the first macroscopic complex organisms in the geological record and may hold the key to our understanding of the origin of animals. Ediacaran macrofossils are as “strange as life on another planet” and have evaded taxonomic classification, with interpretations ranging from marine animals or giant single-celled protists to terrestrial lichens. Here, we show that lipid biomarkers extracted from organically preserved Ediacaran macrofossils unambiguously clarify their phylogeny. Dickinsonia and its relatives solely produced cholesteroids, a hallmark of animals. Our results make these iconic members of the Ediacara biota the oldest confirmed macroscopic animals in the rock record, indicating that the appearance of the Ediacara biota was indeed a prelude to the Cambrian explosion of animal life.

The earliest fossils of animal-like organisms occur in Ediacaran rocks that are approximately 571 million years old. Yet 24-isopropylcholestanes and other C 30 fossil sterol molecules have been suggested to reflect an important ecological role of demosponges as the first abundant animals by the end of the Cryogenian period (>635 million years ago). Here, we demonstrate that C 30 24-isopropylcholestane is not diagnostic for sponges and probably formed in Neoproterozoic sediments through the geological methylation of C 29 sterols of chlorophyte algae, the dominant eukaryotes at that time. These findings reconcile biomarker evidence with the geological record and revert the oldest evidence for animals back into the latest Ediacaran. By subjecting chlorophyte lipid extracts to pyrolysis, the authors demonstrate that the lipid biomarkers 24-isopropylcholestane and 24- n -propylcholestane can be generated from algal C 29 sterol in experiments simulating diagenetic processes, thereby undermining their status as sponge biomarkers.

The Ediacara biota (~575–541 million years ago) mark the emergence of large, complex organisms in the palaeontological record, preluding the radiation of modern animal phyla. However, their phylogenetic relationships, even at the domain level, remain controversial. We report the discovery of molecular fossils from organically preserved specimens of Beltanelliformis , demonstrating that they represent large spherical colonies of cyanobacteria. The conservation of molecular remains in organically preserved Ediacaran organisms opens a new path for unravelling the natures of the Ediacara biota. Organic preserved biomarkers in specimens of Beltanelliformis reveal that these enigmatic members of the Ediacara biota were benthic colonial cyanobacteria.

The dawn of animals remains one of the most mysterious milestones in the evolution of life. The fossil lipids 24-isopropylcholestane and 26-methylstigmastane are considered diagnostic for demosponges—arguably the oldest group of living animals. The widespread occurrence and high relative abundance of these biomarkers in Ediacaran sediments from 635–541 million years (Myr) ago have been viewed as evidence for the rise of animals to ecological importance approximately 100 Myr before their rapid Cambrian radiation. Here we show that the biosynthesis of 24-isopropylcholestane and 26-methylstigmastane precursors is common among early-branching unicellular Rhizaria—heterotrophic protists that play an important role in trophic cycling and carbon export in the modern ocean. Negating these hydrocarbons as sponge biomarkers, our study places the oldest evidence for animals closer to the Cambrian Explosion. Cambrian silica hexactine spicules that are approximately 535 Myr old now represent the oldest diagnostic sponge remains, whereas approximately 558-Myr-old Dickinsonia and Kimberella (Ediacara biota) provide the most reliable evidence for the emergence of animals. The proliferation of predatory protists may have been responsible for much of the ecological changes during the late Neoproterozoic, including the rise of algae, the establishment of complex trophic relationships and the oxygenation of shallow-water habitats required for the subsequent ascent of macroscopic animals. Fossil lipid biomarkers previously thought to be diagnostic of sponges (and thus indicative of animal life) are found to be preserved in unicellular Rhizarian protists, questioning a pre-Cambrian origin of sponges.

Oxygenic photosynthesis is widely accepted as the most important bioenergetic process happening in Earth's surface environment 1 . It is thought to have evolved within the cyanobacterial lineage, but it has been difficult to determine when it began. Evidence based on the occurrence and appearance of stromatolites 2 and microfossils 3 indicates that phototrophy occurred as long ago as 3,465 Myr although no definite physiological inferences can be made from these objects. Carbon isotopes and other geological phenomena 4 , 5 provide clues but are also equivocal. Biomarkers are potentially useful because the three domains of extant life—Bacteria, Archaea and Eukarya—have signature membrane lipids with recalcitrant carbon skeletons. These lipids turn into hydrocarbons in sediments and can be found wherever the recordis sufficiently well preserved. Here we show that 2-methylbacteriohopanepolyols occur in a high proportion of cultured cyanobacteria and cyanobacterial mats. Their 2-methylhopane hydrocarbon derivatives are abundant in organic-rich sediments as old as 2,500 Myr. These biomarkers may help constrain the age of the oldest cyanobacteria and the advent of oxygenic photosynthesis. They could also be used to quantify the ecological importance of cyanobacteria through geological time.