Paleoproterozoic sterol biosynthesis and the rise of oxygen

Gold, David A.; Caron, Abigail M.; Fournier, Gregory P.; Summons, Roger E.

doi:10.1038/nature21412

Cited by 108 publications

(93 citation statements)

References 66 publications

(49 reference statements)

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“…Molecular clock studies (Gold, Caron, Fournier, & Summons, ) predict that sterol synthesis evolved early in eukaryotic evolution significantly prior to the diversification of crown group eukaryotes and that the last eukaryotic common ancestor LECA was probably capable of making sterols (Desmond & Gribaldo, ). In support of this, bacterially derived steroids with methylation preserved at C‐4 (Wei, Yin, & Welander, ) have been reported in immature rocks from ca.…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2019

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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.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2019

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“…Therefore, the reader should interpret the reported age estimates as an approximation, as simulations of plausibility, and as a tool to distinguish between competing hypotheses. Even so, molecular clocks on duplicated proteins have been used informatively before (Aguileta, Bielawski, & Yang, ; Boyd et al., ; Gold, Caron, Fournier, & Summons, ; Sharma & Wheeler, ; Shih & Matzke, ) and our molecular clock is strongly constrained by three pieces of well‐supported and independent evidence: (a) by evidence of photosynthesis at 3.5 Ga, (b) by the fact that all Cyanobacteria and photosynthetic eukaryotes have inherited a standard form of D1, and (c) by the very slow rate of evolution of the core proteins over the Proterozoic. Under these constraints, the divergence between D1 and D2 is better explained by the duplication event occurring early in the evolutionary history of photosynthesis, in the early Archean, with the appearance of standard PSII occurring after a long period of evolutionary innovation.…”

Section: Discussionmentioning

confidence: 98%

Early Archean origin of Photosystem II

et al. 2018

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Photosystem II is a photochemical reaction center that catalyzes the light‐driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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“…Support for this comes from molecular clock estimates of ca. 2310 Ma for the origin of sterol biosynthesis, an oxygen-requiring pathway ( 181 ). …”

Section: A Theoretical Framework For the Evolutionary Timetablementioning

confidence: 99%