Geological alteration of Precambrian steroids mimics early animal signatures

Abstract

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 26methylated steranes-hydrocarbon structures currently attributed to the earliest animals-can form via geological alteration of common algal sterols, which carries important implications for paleo-ecological interpretations and inhibits the use of such unconventional 'sponge' steranes for reconstructing early animal evolution.Determining the first appearance of animals in the rock record places important constraints on the timing and environmental conditions surrounding the Neoproterozoic advent of organismic complexity. In particular the perceived late rise of animals-nearly a billion years after the first fossil eukaryotic cells emerge in the rock record ~1600 million years ago 1,2 (Ma)-remains one of the fundamental unexplained phenomena of evolution. Resolving the drivers for the emergence of organismic complexity fundamentally relies on a reliable temporal framework of animal evolution. In this regard, occurrences of Cambrian sponge spicules [3][4][5] and animal fossils of unspecific affinity (~560 Ma 6 ) are preceded by a much earlier record (up to ~640 Ma 7-9 ) of unconventional fossil steroid lipids (i.e. steranes) considered diagnostic for early sponges and thus for animal-grade life. Timing the rise of complex life thus crucially depends on the applicability of these biomarker hydrocarbons, which warrants thorough scrutinisation.ster-2-ene intermediates 20,21 . Our observation of a nearly identical alkylation pattern in 3and 26-alkylsteranes thus also suggests a diagenetic origin of 26-alkylation. Figure 2. Alkylsteranes in Neoproterozoic rocks and in sterol pyrolysates. Cross plots show the relative distribution of 3-and 26-alkylcholestanes in (a.) the ~740 Ma Chuar Group (#L.39) 40 , and (b.) the 635 Ma Araras Group (#TeS-22) 40 ; see Supplementary Information for sample pedigrees).(c.) The relative distribution pattern of 26alkylsteranes in the Chuar Group matches that in the ~100 Myr younger Araras Group. (d.) C28 sterane (m/z 386217) GC-MS traces show the presence of 26-methylcholestanes (red peaks) in a laboratory pyrolysate (desmosterol, 300ºC, #8 in Supplementary Table 1) and in a Neoproterozoic rock extract (Chuar Group; #L.38), which differ from ergostanes (i.e. 24-methylcholestanes; blue peaks) commonly present in Phanerozoic rocks and oils (here shown in Phanerozoic oil standard NSO-1); also see Supplementary Figure 1. (e.) Pyrolysis of desmosterol creates a series of 26alkylsteranes. Closed circles mark C1-C4 alkylcholestane peaks in same elution position as αααR isomers in Neoproterozoic rock extracts (the identity of the αααR isomer of 26-mec cholestane was additionally confirmed through coelution experiments with an authentic standard); open circles mark consecutive peaks of t...

Current understanding on the Cambrian Explosion: questions and answers

“…If they were validated the molecular record of sponges would be more than 100 Ma prior to the earliest record of siliceous spicules (Antcliffe et al 2014). However, sponge origin of the supposed biomarkers has been challenged by a number of studies (e.g., Antcliffe 2013;Botting and Muir 2018;Botting and Nettersheim 2018;Nettersheim et al 2019;Bobrovskiy et al 2020;van Maldegem et al 2020;Love and Zumberge 2021). In addition, coprostane was proposed as a metazoan biomarker and detected in the iconic Ediacaran fossil Dickinsonia (Bobrovskiy et al 2018).…”

Molecular dating of the blood pigment hemocyanin provides new insight into the origin of animals

“…This assumption is corroborated by molecular estimates (Dohrmann & Wörheide, 2017;dos Reis et al, 2015), the presence of a putative sponge fossil from 890 Ma (Turner, 2021) and diagnostic of pre-Marinoan (<650-635 Ma) demosponges (Love et al, 2009;Love & Summons, 2015), and possible cryostane demosponges biomarkers indigenous to bitumens and oils compatible with pre-Sturtian metazoans (<800-740 Ma) (Brocks et al, 2016). However, new evidence calls into question the veracity of biomarkers from the first metazoans, drawing attention to the fact that they may be algal biomarkers, which are common during the Neoproterozoic (Bobrovskiy et al, 2021;van Maldegem et al, 2021).…”

Bacterial sterol methylation confounds eukaryotic biomarker interpretations

“…Trace amounts of 24-ipc and 26-mes have also been reported in hydrogenated lipid extracts from Rhizaria (31), although attempts to replicate these results have not been successful (23). Subsequent studies demonstrated 24-ipc and 26-mes form abiotically from certain C 29 sterols during laboratory pyrolysis under conditions that may mimic diagenesis (26, 32). These studies suggest that the previously observed Rhizarian 24-isopropyl and 26-methyl steranes may have been generated through laboratory pyrolysis rather than by in vivo synthesis and that Neoproterozoic 24-ipc and 26-mes may have formed abiotically from algal sterols.…”

“…However, the use of 24-ipc and 26-mes as biomarkers for demosponges has been controversial and continues to be debated for several reasons (19)(20)(21)(22)(23)(24)(25)(26). For example, 24-isopropyl sterols have been identified in pelagophyte algae which produce the structurally related compound 24-n-propylcholesterol as their major sterol (27)(28)(29)(30).…”