Absence of biomarker evidence for early eukaryotic life from the Mesoproterozoic Roper Group: Searching across a marine redox gradient in mid‐Proterozoic habitability

Abstract

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.

Free and kerogen‐bound biomarkers from late Tonian sedimentary rocks record abundant eukaryotes in mid‐Neoproterozoic marine communities

“…Consistent with this body of work, recent evidence from lipid biomarker assemblages suggests that primary productivity in Mesoproterozoic oceans (~1,640–1,000 Ma) was consistently dominated by communities rich in bacteria as revealed by a dearth of eukaryotic (4‐desmethyl) sterane biomarkers below detection limits (Figure ; Blumenberg, Thiel, Riegel, Kah, & Reitner, ; Brocks et al, , , ; Flannery & George, ; Gueneli et al, ; Isson et al, ; Luo, Hallmann, Xie, Ruan, & Summons, ; Nguyen et al, ; Suslova, Parfenova, Saraev, & Nagovitsyn, ) prior to the first detection of extractable eukaryotic biomarkers in Neoproterozoic rocks appearing from ca. 800 Ma and younger (Brocks et al, ; Grosjean, Love, Stalvies, Fike, & Summons, ; Isson et al, ; Love et al, ; van Maldegem et al, ).…”

“…Alternatively, other low‐oxygen‐adapted eukaryotes (Takishita et al, ) or certain bacteria (Peters et al, ) are also plausible sources of gammacerane (and methylgammaceranes). These alternative sources could explain the trace finite amounts of gammacerane detected in Mesoproterozoic rocks from the Roper Group (Nguyen et al, ). The polycyclic terpane biomarker assemblages are likely indicative of late Tonian marine communities, which locally could be rich in eukaryotic organisms, including eukaryotic primary producers and consumers, and which were substantially different to the bacterially dominated communities supported in Mesoproterozoic ocean systems.…”

“…The abundance ratio of the major (C 27 –C 35 ) hopanes to (C 27 –C 29 ) regular steranes provides a direct and informative measure of the relative contributions of bacteria and eukaryotes to sedimentary organic matter, which has proved useful to track the evolving Proterozoic surface ocean ecology. A temporal step change occurs as sterane/hopane (S/H) ratios shift from values of approximately zero (0.00) throughout the Paleoproterozoic and Mesoproterozoic as revealed by a dearth of eukaryotic steranes (Blumenberg et al, ; Brocks et al, , , ; Flannery & George, ; Gueneli et al, ; Isson et al, ; Luo et al, ; Nguyen et al, ; Suslova et al, ) before obviously increasing significantly during the Cryogenian and Ediacaran Periods (Brocks et al, ; Grosjean et al, ; Love et al, ; Stolper et al, ). In some cases, these can attain Phanerozoic average S/H range of ~0.5–2.0 for sedimentary rocks and oils, although bacterially dominated Ediacaran biomarker assemblages (with S/H values < 0.1) are also found in other locations and can feature for tens of millions of years (Pehr et al, ).…”

“…Routine recovery and analysis of the kerogen‐bound biomarkers was performed here via the tested method of continuous‐flow hydropyrolysis (HyPy) on the solvent‐extracted rock residues (Bishop, Love, McAulay, Snape, & Farrimond, ; Love et al, , ; Love, McAulay, Snape, & Bishop, ; Meredith, Snape, & Love, ). HyPy of kerogen is a valuable approach for testing the syngenicity of biomarker compounds in Precambrian rocks (Love et al, ; Nguyen et al, ; Zumberge et al, ), and it was a key analytical strategy that verified that polycyclic biomarker alkanes previously reported from overmature Archean and early Proterozoic rocks were exogenous trace contaminants (French et al, ). Alternative analytical approaches that scrutinize for exogenous biomarker components include the comparison of the exterior versus interior rock bitumen portion (E/I) compositions, which have been successfully employed on rocks of this age (Brocks et al, , ), although these methods can only recover biomarkers from the soluble organic matter phase (bitumen) and not from the kerogen.…”

“…Lipid biomarker assemblages recovered from thermally well‐preserved sedimentary rocks can help unravel the temporal dynamics associated with the protracted emergence, diversification, and ecological expansion of Eukarya across the Proterozoic Eon (2,500–541 Ma) and may be used to assess the quantitative impact of early eukaryotes within ancient marine communities (Brocks et al, , , ; Dutkiewicz, Volk, Ridley, & George, ; Gallagher et al, ; Isson et al, ; Love et al, ; Luo, George, Xu, & Zhong, ; Nguyen et al, ). The mid‐Proterozoic (1,800–1,000 Ma) was characterized by a remarkably long period of biogeochemical, tectonic, and climatic stability, with marine community structures buffered by feedback operating within coupled nutrient–carbon cycles imposed on primary production in the surface ocean (Cole et al, ; Crockford et al, ; Hardisty et al, ; Holland, ; Lyons, Reinhard, & Planavsky, ; Ozaki, Reinhard, & Tajika, ; Planavsky et al, , ; Poulton & Canfield, ).…”