No abstract

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.oxygenic photosynthesis | eukaryotes | cyanobacteria | Great Oxidation Event | Pilbara

he transition from unicellular protists to multicellular animals constitutes one of the most intriguing and enigmatic events in the evolutionary history of life, largely due to the absence of unambiguous physical fossils for the earliest fauna. The Neoproterozoic rise of eukaryotes 1 , including demosponges 2 , in marine environments can be discerned from lipid biomarker records preserved in ancient sedimentary rocks that have experienced a mild thermal history. Molecular phylogenies commonly show that sponges (Porifera) are the sister group of other animals 3 and molecular evidence for Neoproterozoic animal life was first proposed based on the occurrence of unusual C 30 demosponge-derived steranes informally known as 24-isopropylcholestane (24-ipc) steranes in sedimentary rocks and oils of that age 2,4. These steranes are the hydrocarbon remains of 24-isopropylcholesterols and structurally related sterols 5. The record of 24-ipc steranes commences in Cryogenian-aged sediments in South Oman (around 717-635 million years ago (Ma) 2,6) and then occurs continuously through the Ediacaran-Cambrian formations of the Huqf Supergroup of the South Oman Salt Basin. Notably, these steroids also occur as covalently bound constituents fixed within the immobile kerogen phase of the same rocks, which is an important confirmation that these are not younger contaminant compounds that migrated into the rocks 2. Demosponges are the only known extant taxon that can biosynthesize 24-ipc precursors as their major sterols. High relative absolute abundances of 24-ipc steranes have now been reported in many other late Neoproterozoic-early Cambrian rocks and oils 2,4,7-9. These 24-ipc occurrences-if interpreted correctly-reflect an early presence of Porifera and provide a conservative minimum time estimate for the origin of animal multicellularity and the sponge body plan. Others have hypothesized that the 24-ipc steranes could be derived from unicellular animal ancestors or have an algal origin 10 since the parent sterols have been reported in trace amounts in some extant pelagophyte algae 2. The claim that poribacterial sponge symbionts from the candidate phylum Poribacteria can make 24-ipc steroids 11 has since been shown to be erroneous due to a genome assembly error 12,13. Currently, two chromatographically resolvable series of ancient C 30 steranes are known: 24-n-propylcholestane (24-npc) and 24-ipc. Demosponges are the most plausible Neoproterozoic-Cambrian source of 24-npc as well as 24-ipc because both are produced by extant demosponges 2. Foraminifera are another possible source of 24-npc 14. Pelagophyte algae probably account for the 24-npc steranes that are found in Devonian and younger marine sediments and their derived oils 13. Various recent findings support a pre-Ediacaran origin of animals and sponges, and arguably reinforce the validity of the 24-ipc biomarker record, including: (1) steroid assays and genomic analyses of extant taxa 13 , which suggest that sponges were the most likely Neoproterozoic source biota for 24-...

By about 2.0 billion years ago (Ga), there is evidence for a period best known for its extended, apparent geochemical stability expressed famously in the carbonate–carbon isotope data. Despite the first appearance and early innovation among eukaryotic organisms, this period is also known for a rarity of eukaryotic fossils and an absence of organic biomarker fingerprints for those organisms, suggesting low diversity and relatively small populations compared to the Neoproterozoic era. Nevertheless, the search for diagnostic biomarkers has not been performed with guidance from paleoenvironmental redox constrains from inorganic geochemistry that should reveal the facies that were most likely hospitable to these organisms. Siltstones and shales obtained from drill core of the ca. 1.3–1.4 Ga Roper Group from the McArthur Basin of northern Australia provide one of our best windows into the mid‐Proterozoic redox landscape. The group is well dated and minimally metamorphosed (of oil window maturity), and previous geochemical data suggest a relatively strong connection to the open ocean compared to other mid‐Proterozoic records. Here, we present one of the first integrated investigations of Mesoproterozoic biomarker records performed in parallel with established inorganic redox proxy indicators. Results reveal a temporally variable paleoredox structure through the Velkerri Formation as gauged from iron mineral speciation and trace‐metal geochemistry, vacillating between oxic and anoxic. Our combined lipid biomarker and inorganic geochemical records indicate at least episodic euxinic conditions sustained predominantly below the photic zone during the deposition of organic‐rich shales found in the middle Velkerri Formation. The most striking result is an absence of eukaryotic steranes (4‐desmethylsteranes) and only traces of gammacerane in some samples—despite our search across oxic, as well as anoxic, facies that should favor eukaryotic habitability and in low maturity rocks that allow the preservation of biomarker alkanes. The dearth of Mesoproterozoic eukaryotic sterane biomarkers, even within the more oxic facies, is somewhat surprising but suggests that controls such as the long‐term nutrient balance and other environmental factors may have throttled the abundances and diversity of early eukaryotic life relative to bacteria within marine microbial communities. Given that molecular clocks predict that sterol synthesis evolved early in eukaryotic history, and (bacterial) fossil steroids have been found previously in 1.64 Ga rocks, then a very low environmental abundance of eukaryotes relative to bacteria is our preferred explanation for the lack of regular steranes and only traces of gammacerane in a few samples. It is also possible that early eukaryotes adapted to Mesoproterozoic marine environments did not make abundant steroid lipids or tetrahymanol in their cell membranes.

Nettersheim et al. 1 propose that unicellular Rhizaria are the likely biological source of the C 30 steroidal hydrocarbons found abundantly in Neoproterozoic-Cambrian sedimentary rocks. Their hypothesis challenges earlier research arguing that 24-isopropylcholestane (24ipc) and 26-methylstigmastane (26-mes) are produced by demosponges and, therefore, early animal biomarkers 2-4. Fundamental problems beset the new steroid biomarker data and its interpretation 1. The primary problem is one of mass balance. C 30 steranes typically account for ~3%, on average, of the total C 27-C 30 steranes in many Neoproterozoic rocks and oils 2,4 with 24-ipc, alone, accounting for >1% of the total sterane signal. Since all sterols typically follow similar preservation pathways, the carbon number distributions of C 27-C 30 steranes in the geological record should closely match proportions of sterol precursors of the source biota. Accordingly, plausible biological sources of ancient 24-ipc and 26-mes sterols must have Reprints and permissions information is available at www.nature.com/reprints.