Rapid encapsulation of true ferns and arborane/fernane compounds fossilised in siderite concretions supports analytical distinction of plant fossils.

Fossilised true ferns (Pecopteris sp.) preserved in siderite concretions from the Mazon Creek Lagerstätte (Illinois) presented a unique opportunity to characterise the organic signatures of these late Carboniferous plants. Localised analyses of true fern fossils showed several highly abundant phytohopanoids and fernane/arborane derived aromatic products, which were present only negligibly within their siderite matrix, as well as from other types of fossilised plants. These terpenoids had been recognised in some extant ferns, but scarcely in sedimentary organic matter and their exact source remained ambiguous. The present fossil biomarker data confirms an ancient true fern origin. Furthermore, the excellent concretion preservation of a series of related terpenoid products provided a rare insight into their diagenetic formation. The benign properties of carbonate concretions could be exploited further for biomarker evidence of other fossilised organisms, with one important caveat being that biomarker signals attributed to isolated fossils be significantly distinct from background organic matter pervading the concretion matrix. For instance, hydrocarbon profiles of seed ferns (pteridosperms) and articulates (horsetails) also preserved in Mazon Creek concretions were indistinguishable from separate analysis of their concretion matrix, preventing biomarker recognition.

Genetics re-establish the utility of 2-methylhopanes as cyanobacterial biomarkers before 750 million years ago.

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 B12. 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.

Early sea ice decline off East Antarctica at the last glacial-interglacial climate transition.

Antarctic climate warming and atmospheric CO2 rise during the last deglaciation may be attributed in part to sea ice reduction in the Southern Ocean. Yet, glacial-interglacial Antarctic sea ice dynamics and underlying mechanisms are poorly constrained, as robust sea ice proxy evidence is sparse. Here, we present a molecular biomarker-based sea ice record that resolves the spring/summer sea ice variability off East Antarctica during the past 40 thousand years (ka). Our results indicate that substantial sea ice reduction culminated rapidly and contemporaneously with upwelling of carbon-enriched waters in the Southern Ocean at the onset of the last deglaciation but began at least ~2 ka earlier probably driven by an increasing local integrated summer insolation. Our findings suggest that sea ice reduction and associated feedbacks facilitated stratification breakup and outgassing of CO2 in the Southern Ocean and warming in Antarctica but may also have played a leading role in initializing these deglacial processes in the Southern Hemisphere.

Biological diversification linked to environmental stabilization following the Sturtian Snowball glaciation.

The body fossil and biomarker records hint at an increase in biotic complexity between the two Cryogenian Snowball Earth episodes (ca. 661 million to ≤650 million years ago). Oxygen and nutrient availability can promote biotic complexity, but nutrient (particularly phosphorus) and redox dynamics across this interval remain poorly understood. Here, we present high-resolution paleoredox and phosphorus phase association data from multiple globally distributed drill core records through the non-glacial interval. These data are first correlated regionally by litho- and chemostratigraphy, and then calibrated within a series of global chronostratigraphic frameworks. The combined data show that regional differences in postglacial redox stabilization were partly controlled by the intensity of phosphorus recycling from marine sediments. The apparent increase in biotic complexity followed a global transition to more stable and less reducing conditions in shallow to mid-depth marine environments and occurred within a tolerable climatic window during progressive cooling after post-Snowball super-greenhouse conditions.

Lost world of complex life and the late rise of the eukaryotic crown.

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 sterols1,2. 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 years3. 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 Bloch4. 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.

Some animals make plant sterols.

Most animals abandoned plant sterols early in evolution, but some still depend on them.

Guts, gut contents, and feeding strategies of Ediacaran animals.

The oldest animals appear in the fossil record among Ediacara biota communities. They prelude animal-dominated ecosystems of the Phanerozoic and may hold clues to the appearance of modern animal phyla in the Cambrian explosion. However, little is known about the phylogeny of the Ediacaran organisms and even less about their diet and feeding behavior.1,2,3 An exception is mollusc-like Kimberella, for which a fossilized gut, feeding traces, and even potential coprolites have been found.4,5 By contrast, Ediacaran organic-walled tubes, such as Sabellidites and Calyptrina, are thought to belong to tube worms comparable with modern Siboglinidae that have no gut but gain their nutrition from symbiotic bacteria.6,7 Here, we examine the gut contents of Ediacaran animals using biomarker molecules. We show that 558-million-year (Ma)-old tube worm-like Calyptrina and mollusc-like Kimberella possessed a gut and shared a diet of green algae and bacteria. Despite their ancient age, sterol metabolism within the gut of both organisms was already comparable to extant invertebrates.8Dickinsonia, one of the key Ediacaran animals, show no traces of dietary molecules, indicating a different feeding mode and possible external digestion analogous to modern Placozoa. Lipid biomarkers uncover a range of feeding strategies in Ediacaran communities, highlighting true eumetazoan physiology of some Ediacaran animals.

Fossil Biomarkers and Biosignatures Preserved in Coprolites Reveal Carnivorous Diets in the Carboniferous Mazon Creek Ecosystem.

The reconstruction of ancient trophic networks is pivotal to our understanding of ecosystem function and change through time. However, inferring dietary relationships in enigmatic ecosystems dominated by organisms without modern analogues, such as the Carboniferous Mazon Creek fauna, has previously been considered challenging: preserved coprolites often do not retain sufficient morphology to identify the dietary composition. Here, we analysed n = 3 Mazon Creek coprolites in concretions for dietary signals in preserved biomarkers, stable carbon isotope data, and macromolecular composition. Cholesteroids, metazoan markers of cholesterol, show an increased abundance in the sampled coprolites (86 to 99% of the total steranes) compared to the surrounding sediment, indicating an endogenous nature of preserved organics. Presence of unaltered 5α-cholestan-3ß-ol and coprostanol underline the exceptional molecular preservation of the coprolites, and reveal a carnivorous diet for the coprolite producer. Statistical analyses of in situ Raman spectra targeting coprolite carbonaceous remains support a metazoan affinity of the digested fossil remains, and suggest a high trophic level for the coprolite producer. These currently oldest, intact dietary stanols, combined with exquisitely preserved macromolecular biosignatures in Carboniferous fossils offer a novel source of trophic information. Molecular and biosignature preservation is facilitated by rapid sedimentary encapsulation of the coprolites within days to months after egestion.

Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae.

The acquisition of photosynthesis is a fundamental step in the evolution of eukaryotes. However, few phototrophic organisms are unambiguously recognized in the Precambrian record. The in situ detection of metabolic byproducts in individual microfossils is the key for the direct identification of their metabolisms. Here, we report a new integrative methodology using synchrotron-based X-ray fluorescence and absorption. We evidence bound nickel-geoporphyrins moieties in low-grade metamorphic rocks, preserved in situ within cells of a ~1 Gyr-old multicellular eukaryote, Arctacellularia tetragonala. We identify these moieties as chlorophyll derivatives, indicating that A. tetragonala was a phototrophic eukaryote, one of the first unambiguous algae. This new approach, applicable to overmature rocks, creates a strong new proxy to understand the evolution of phototrophy and diversification of early ecosystems.

Geological alteration of Precambrian steroids mimics early animal signatures.

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.

Algal origin of sponge sterane biomarkers negates the oldest evidence for animals in the rock record.

The earliest fossils of animal-like organisms occur in Ediacaran rocks that are approximately 571 million years old. Yet 24-isopropylcholestanes and other C30 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 C30 24-isopropylcholestane is not diagnostic for sponges and probably formed in Neoproterozoic sediments through the geological methylation of C29 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.

Discovery of the oldest known biomarkers provides evidence for phototrophic bacteria in the 1.73 Ga Wollogorang Formation, Australia.

The discovery of mid-Proterozoic (1.8-0.8 billion years ago, Ga) indigenous biomarkers is a challenge, since biologically informative molecules of such antiquity are commonly destroyed by metamorphism or overprinted by drilling fluids and other anthropogenic petroleum products. Previously, the oldest clearly indigenous biomarkers were reported from the 1.64 Ga Barney Creek Formation in the northern Australian McArthur Basin. In this study, we present the discovery of biomarker molecules from carbonaceous shales of the 1.73 Ga Wollogorang Formation in the southern McArthur Basin, extending the biomarker record back in time by ~90 million years. The extracted hydrocarbons illustrate typical mid-Proterozoic signatures with a large unresolved complex mixture, high methyl alkane/n-alkane ratios and the absence of eukaryotic steranes. Acyclic isoprenoids, saturated carotenoid derivatives, bacterial hopanes and aromatic hopanoids and steroids also were below detection limits. However, continuous homologous series of low molecular weight C14 -C19 2,3,4- and 2,3,6-trimethyl aryl isoprenoids (AI) were identified, and C20 -C22 AI homologues were tentatively identified. Based on elevated abundances relative to abiogenic isomers, we interpret the 2,3,6-AI isomer series as biogenic molecules and the 2,3,4-AI series as possibly biogenic. The biological sources for the 2,3,6-AI series include carotenoids of cyanobacteria and/or green sulphur bacteria (Chlorobiaceae). The lower concentrated 2,3,4-AI series may be derived from purple sulphur bacteria (Chromatiaceae). These degradation products of carotenoids are the oldest known clearly indigenous molecules of likely biogenic origin.

Food sources for the Ediacara biota communities.

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.

Putative sponge biomarkers in unicellular Rhizaria question an early rise of animals.

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.

Simple sediment rheology explains the Ediacara biota preservation.

The soft-bodied Ediacara biota (571-541 million years ago) represents the oldest complex large organisms in the fossil record, providing a bridge between largely microbial ecosystems of the Precambrian and the animal-dominated world of the Phanerozoic, potentially holding clues about the early evolution of Metazoa. However, the nature of most Ediacaran organisms remains unresolved, partly due to their enigmatic non-actualistic preservation. Here, we show that Flinders-style fossilization of Ediacaran organisms was promoted by unusually prolonged conservation of organic matter, coupled with differences in rheological behaviour of the over- and underlying sediments. In contrast with accepted models, cementation of overlying sand was not critical for fossil preservation, which is supported by the absence of cement in unweathered White Sea specimens and observations of soft sediment deformation in South Australian specimens. The rheological model, confirmed by laboratory simulations, implies that Ediacaran fossils do not necessarily reflect the external shape of the organism, but rather the morphology of a soft external or internal organic 'skeleton'. The rheological mechanism provides new constraints on biological interpretations of the Ediacara biota.

Microbial assemblage and palaeoenvironmental reconstruction of the 1.38 Ga Velkerri Formation, McArthur Basin, northern Australia.

The ca. 1.38 billion years (Ga) old Roper Group of the McArthur Basin, northern Australia, is one of the most extensive Proterozoic hydrocarbon-bearing units. Organic-rich black siltstones from the Velkerri Formation were deposited in a deep-water sequence and were analysed to determine their organic geochemical (biomarker) signatures, which were used to interpret the microbial diversity and palaeoenvironment of the Roper Seaway. The indigenous hydrocarbon biomarker assemblages describe a water column dominated by bacteria with large-scale heterotrophic reworking of the organic matter in the water column or bottom sediment. Possible evidence for microbial reworking includes a large unresolved complex mixture (UCM), high ratios of mid-chained and terminally branched monomethyl alkanes relative to n-alkanes-features characteristic of indigenous Proterozoic bitumen. Steranes, biomarkers for single-celled and multicellular eukaryotes, were below detection limits in all extracts analysed, despite eukaryotic microfossils having been previously identified in the Roper Group, albeit largely in organically lean shallower water facies. These data suggest that eukaryotes, while present in the Roper Seaway, were ecologically restricted and contributed little to export production. The 2,3,4- and 2,3,6-trimethyl aryl isoprenoids (TMAI) were absent or in very low concentration in the Velkerri Formation. The low abundance is primary and not caused by thermal destruction. The combination of increased dibenzothiophene in the Amungee Member of the Velkerri Formation and trace metal redox geochemistry suggests that degradation of carotenoids occurred during intermittent oxygen exposure at the sediment-water interface and/or the water column was rarely euxinic in the photic zone and likely only transiently euxinic at depth. A comparison of this work with recently published biomarker and trace elemental studies from other mid-Proterozoic basins demonstrates that microbial environments, water column geochemistry and basin redox were heterogeneous.

Ancient steroids establish the Ediacaran fossil Dickinsonia as one of the earliest animals.

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.

Molecular fossils from organically preserved Ediacara biota reveal cyanobacterial origin for Beltanelliformis.

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.