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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.

Eukaryotic algae rose to ecological relevance after the Neoproterozoic Snowball Earth glaciations, but the causes for this consequential evolutionary transition remain enigmatic. Cap carbonates were globally deposited directly after these glaciations, but they are usually organic barren or thermally overprinted. Here we show that uniquely-preserved cap dolostones of the Araras Group contain exceptional abundances of a newly identified biomarker: 25,28-bisnorgammacerane. Its secular occurrence, carbon isotope systematics and co-occurrence with other demethylated terpenoids suggest a mechanistic connection to extensive microbial degradation of ciliate-derived biomass in bacterially dominated ecosystems. Declining 25,28-bisnorgammacerane concentrations, and a parallel rise of steranes over hopanes, indicate the transition from a bacterial to eukaryotic dominated ecosystem after the Marinoan deglaciation. Nutrient levels already increased during the Cryogenian and were a prerequisite, but not the ultimate driver for the algal rise. Intense predatory pressure by bacterivorous protists may have irrevocably cleared self-sustaining cyanobacterial ecosystems, thereby creating the ecological opportunity that allowed for the persistent rise of eukaryotic algae to global importance. It remains unclear when and why the world’s oceans, once largely occupied by bacteria, became dominated by photosynthetic algae. Here, using fossil lipids in million year old rocks, the authors show that predation after the Snowball Earth glaciations created the opportunity for a global shift to algal ecosystems.

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 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.

Fossilized lipids offer a rare glimpse into ancient ecosystems. 2-Methylhopanes in sedimentary rocks were once used to infer the importance of cyanobacteria as primary producers throughout geological history. However, the discovery of hopanoid C-2 methyltransferase (HpnP) in Alphaproteobacteria led to the downfall of this molecular proxy. In the present study, we re-examined the distribution of HpnP in a new phylogenetic framework including recently proposed candidate phyla and re-interpreted a revised geological record of 2-methylhopanes based on contamination-free samples. We show that HpnP was probably present in the last common ancestor of cyanobacteria, while the gene appeared in Alphaproteobacteria only around 750 million years ago (Ma). A subsequent rise of sedimentary 2-methylhopanes around 600 Ma probably reflects the expansion of Alphaproteobacteria that coincided with the rise of eukaryotic algae—possibly connected by algal dependency on microbially produced vitamin B 12 . Our findings re-establish 2-methylhopanes as cyanobacterial biomarkers before 750 Ma and thus as a potential tool to measure the importance of oxygenic cyanobacteria as primary producers on early Earth. Our study illustrates how genetics can improve the diagnostic value of biomarkers and refine the reconstruction of early ecosystems. Using phylogenetic analysis of a hopanoid-producing gene in bacteria, the authors establish fossil 2-methylhopanes as lipid biomarkers for aerobic cyanobacteria and reveal the role of cyanobacteria in primary production before 750 million years ago.

The absence of unambiguous animal body fossils in rocks older than the late Ediacaran has rendered fossil lipids the most promising tracers of early organismic complexity. Yet much debate surrounds the various potential biological sources of putative metazoan steroids found in Precambrian rocks. Here we show that 26-methylated steranes—hydrocarbon structures currently attributed to the earliest animals—can form via geological alteration of common algal sterols, which carries important implications for palaeo-ecological interpretations and inhibits the use of such unconventional ‘sponge’ steranes for reconstructing early animal evolution. Via congruent observations in geological samples and pyrolysis experiments, the authors demonstrate that 26-alkylsteranes posited as sponge biomarkers can form during diagenesis of common algal sterols.

Sponges are believed by many researchers to be the earliest living animal group, but there is conflicting evidence for the timing of their origin. A molecular fossil discovery supports the contention that sponges appeared very early, but starkly contradicts the body fossil record.