When did oxygenic photosynthesis evolve?

Abstract

The atmosphere has apparently been oxygenated since the 'Great Oxidation Event' ca 2.4 Ga ago, but when the photosynthetic oxygen production began is debatable. However, geological and geochemical evidence from older sedimentary rocks indicates that oxygenic photosynthesis evolved well before this oxygenation event. Fluid-inclusion oils in ca 2.45 Ga sandstones contain hydrocarbon biomarkers evidently sourced from similarly ancient kerogen, preserved without subsequent contamination, and derived from organisms producing and requiring molecular oxygen. Mo and Re abundances and sulphur isotope systematics of slightly older (2.5 Ga) kerogenous shales record a transient pulse of atmospheric oxygen. As early as ca 2.7 Ga, stromatolites and biomarkers from evaporative lake sediments deficient in exogenous reducing power strongly imply that oxygen-producing cyanobacteria had already evolved. Even at ca 3.2 Ga, thick and widespread kerogenous shales are consistent with aerobic photoautrophic marine plankton, and U-Pb data from ca 3.8 Ga metasediments suggest that this metabolism could have arisen by the start of the geological record. Hence, the hypothesis that oxygenic photosynthesis evolved well before the atmosphere became permanently oxygenated seems well supported.

Figure 1

(a) Biomolecules and their (b) geological biomarker derivatives for all three domains of life, including 2α-methylhopane and the sterane stignastane.

Figure 2

Hydrocarbon distributions in organic-rich and organic-poor rocks from a drill-core through the Archaean upper Fortescue and lower Hamersley Groups of the Pilbara Craton, Australia (modified from Brocks et al. 1999).

Figure 3

Stratigraphy of the Huronian Supergroup, Canada, showing the position of the Matinenda Formation below the earliest Palaeoproterozoic glaciation and the first evidence of permanent atmospheric oxygenation in the form of red beds (modified from Dutkiewicz et al. 2006).

Figure 4

Matinenda Formation fluid inclusions showing the distribution of volatile components, (a) UV epifluorescence showing fluorescent oil and (b) plane-polarized light showing gas bubbles (modified from Dutkiewicz et al. 2006).

Figure 5

Entrapment model for Matinenda Formation fluid inclusions. (a) Deposition ca 2.45 Ga, (b) oil migration and (c) metamorphism ca 2.2 Ga (modified from Buick et al. 1998).

Figure 6

Gas chromatograph–mass spectrometry traces for Matinenda Formation fluid-inclusion hydrocarbons. (a) Steranes and (b) hopanes—inset shows methylhopanes (modified from George et al. 2008).

Figure 7

Redox-sensitive trace metal data (modified from Anbar et al. 2007) and sulphur isotopic values (modified from Kaufman et al. 2007) from the ca 2.5 Ga Mt McRae Formation, Hamersley Group, Pilbara Craton, Australia.

Figure 8

Δ³³S_sulphide values through time (modified from Farquhar et al. 2007); note values of less than ±0.25 ppt after ca 2.3 Ga and greater than ±0.25 ppt between 2.8 and 3.0 Ga.

Figure 9

(a–d) Lacustrine stromatolites from the ca 2.72 Ga Tumbiana Formation, Fortescue Group, Pilbara Craton, Australia (modified from Buick 1992).