Reassessing the first appearance of eukaryotes and cyanobacteria

The evolution of oxygenic photosynthesis had a profound impact on the Earth’s surface chemistry, leading to a sharp rise in atmospheric oxygen between 2.45 and 2.32 billion years (Gyr) ago and the onset of extreme ice ages. The oldest widely accepted evidence for oxygenic photosynthesis has come from hydrocarbons extracted from ∼2.7-Gyr-old shales in the Pilbara Craton, Australia, which contain traces of biomarkers (molecular fossils) indicative of eukaryotes and suggestive of oxygen-producing cyanobacteria. The soluble hydrocarbons were interpreted to be indigenous and syngenetic despite metamorphic alteration and extreme enrichment (10–20‰) of 13C relative to bulk sedimentary organic matter. Here we present micrometre-scale, in situ 13C/12C measurements of pyrobitumen (thermally altered petroleum) and kerogen from these metamorphosed shales, including samples that originally yielded biomarkers. Our results show that both kerogen and pyrobitumen are strongly depleted in 13C, indicating that indigenous petroleum is 10–20‰ lighter than the extracted hydrocarbons. These results are inconsistent with an indigenous origin for the biomarkers. Whatever their origin, the biomarkers must have entered the rock after peak metamorphism ∼2.2 Gyr ago and thus do not provide evidence for the existence of eukaryotes and cyanobacteria in the Archaean eon. The oldest fossil evidence for eukaryotes and cyanobacteria therefore reverts to 1.78–1.68 Gyr ago and ∼2.15 Gyr ago, respectively. Our results eliminate the evidence for oxygenic photosynthesis ∼2.7 Gyr ago and exclude previous biomarker evidence for a long delay (∼300 million years) between the appearance of oxygen-producing cyanobacteria and the rise in atmospheric oxygen 2.45–2.32 Gyr ago.

[1]  D. Canfield THE EARLY HISTORY OF ATMOSPHERIC OXYGEN: Homage to Robert M. Garrels , 2005 .

[2]  R Buick,et al.  Archean molecular fossils and the early rise of eukaryotes. , 1999, Science.

[3]  R. C. Morris,et al.  Could bacteria have formed the Precambrian banded iron formations , 2002 .

[4]  I. Fletcher,et al.  NanoSIMS μm-scale in situ measurement of 13C/12C in early Precambrian organic matter, with permil precision , 2008 .

[5]  C. Boreham,et al.  Petroleum Geology and Geochemistry of Middle Proterozoic McArthur Basin, Northern Australia II: Assessment of Source Rock Potential , 1988 .

[6]  Todd A. Ehlers,et al.  REVIEWS IN MINERALOGY AND GEOCHEMISTRY , 2005 .

[7]  J. William Schopf,et al.  Earth's earliest biosphere : its origin and evolution , 1983 .

[8]  Roger E. Summons,et al.  Composition and syngeneity of molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Pilbara Craton, Western Australia , 2003 .

[9]  D. Canfield,et al.  THE EARLY HISTORY OF ATMOSPHERIC OXYGEN , 2005 .

[10]  R. Kopp,et al.  The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Roger E. Summons,et al.  Petroleum geology and geochemistry of the Middle Proterozoic McArthur Basin, Northern Australia: III. Composition of extractable hydrocarbons , 1988 .

[12]  Timothy M. Lenton,et al.  Bistability of atmospheric oxygen and the Great Oxidation , 2006, Nature.

[13]  Roger E. Summons,et al.  A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia , 2003 .

[14]  A. Rousse,et al.  Precise in situ measurements of isotopic abundances with pulse counting of sputtered ions , 2001 .

[15]  K. Hinrichs Microbial fixation of methane carbon at 2.7 Ga: Was an anaerobic mechanism possible? , 2002 .

[16]  I. Fletcher,et al.  Isotopic dating of the migration of a low-grade metamorphic front during orogenesis , 2005 .

[17]  Laura S. Sherman,et al.  Improved methods for isolating and validating indigenous biomarkers in Precambrian rocks , 2007 .

[18]  I. Fletcher,et al.  Prolonged history of episodic fluid flow in giant hematite ore bodies: Evidence from in situ U Pb geochronology of hydrothermal xenotime , 2007 .

[19]  H. Volk,et al.  Preservation of hydrocarbons and biomarkers in oil trapped inside fluid inclusions for >2 billion years , 2008 .

[20]  H. Volk,et al.  Biomarkers from Huronian oil-bearing fluid inclusions: An uncontaminated record of life before the Great Oxidation Event , 2006 .

[21]  G. Slodziana,et al.  QSA influences on isotopic ratio measurements , 2004 .

[22]  J. Brocks,et al.  Assessing biomarker syngeneity using branched alkanes with quaternary carbon (BAQCs) and other plastic contaminants , 2008 .

[23]  L. Kump,et al.  Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago , 2007, Nature.

[24]  Roger E. Summons,et al.  2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis , 1999, Nature.

[25]  S. Bengtson Early life on earth , 1994 .

[26]  A. Knoll,et al.  Eukaryotic organisms in Proterozoic oceans , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  J. Hunt,et al.  Petroleum Geochemistry and Geology , 1995 .

[28]  A. Bekker,et al.  Dating the rise of atmospheric oxygen , 2004, Nature.

[29]  B. Rasmussen Evidence for pervasive petroleum generation and migration in 3.2 and 2.63 Ga shales , 2005 .

[30]  Raymond E. Smith,et al.  Burial metamorphism in the Hamersley Basin, Western Australia , 1982 .

[31]  A. J. Kaufman,et al.  A Whiff of Oxygen Before the Great Oxidation Event? , 2007, Science.

[32]  J. Brocks,et al.  Okenane, a biomarker for purple sulfur bacteria (Chromatiaceae), and other new carotenoid derivatives from the 1640 Ma Barney Creek Formation , 2008 .

[33]  H. Hofmann Precambrian microflora, Belcher Islands, Canada; significance and systematics , 1976 .