Abstract
This article examines the geological evidence for the rise of atmospheric oxygen and the origin of oxygenic photosynthesis. The evidence for the rise of atmospheric oxygen places a minimum time constraint before which oxygenic photosynthesis must have developed, and was subsequently established as the primary control on the atmospheric oxygen level. The geological evidence places the global rise of atmospheric oxygen, termed the Great Oxidation Event (GOE), between ~2.45 and ~2.32 Ga, and it is captured within the Duitschland Formation, which shows a transition from mass-independent to mass-dependent sulfur isotope fractionation. The rise of atmospheric oxygen during this interval is closely associated with a number of environmental changes, such as glaciations and intense continental weathering, and led to dramatic changes in the oxidation state of the ocean and the seawater inventory of transition elements. There are other features of the geologic record predating the GOE by as much as 200–300 million years, perhaps extending as far back as the Mesoarchean–Neoarchean boundary at 2.8 Ga, that suggest the presence of low level, transient or local, oxygenation. If verified, these features would not only imply an earlier origin for oxygenic photosynthesis, but also require a mechanism to decouple oxygen production from oxidation of Earth’s surface environments. Most hypotheses for the GOE suggest that oxygen production by oxygenic photosynthesis is a precondition for the rise of oxygen, but that a synchronous change in atmospheric oxygen level is not required by the onset of this oxygen source. The potential lag-time in the response of Earth surface environments is related to the way that oxygen sinks, such as reduced Fe and sulfur compounds, respond to oxygen production. Changes in oxygen level imply an imbalance in the sources and sinks for oxygen. Changes in the cycling of oxygen have occurred at various times before and after the GOE, and do not appear to require corresponding changes in the intensity of oxygenic photosynthesis. The available geological constraints for these changes do not, however, disallow a direct role for this metabolism. The geological evidence for early oxygen and hypotheses for the controls on oxygen level are the basis for the interpretation of photosynthetic oxygen production as examined in this review.
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Notes
We include all sulfur species with sulfate here because of the possibility of their atmospheric contribution to the Archean sulfur cycle.
The delta notation (e.g., δ13C, δ15N values) describes the permil level deviation of an isotope ratio in a sample from that in a reference material. Equations for these notations are: δ13C = ((13C/12C)sample/(13C/12C)reference − 1) and δ15N = ((15N/14N)sample/(15N/14N)reference − 1).
The delta notation (δ34S) describes the permil level deviation of an isotope ratio in a sample from that in a reference material, and the capital delta notation (Δ33S and Δ36S) describes the deviation of an isotope ratio from a reference fractionation array. Equations for these quantities are: δ34S = (34S/32S)sample/(34S/32S)reference − 1) and Δ33S = (33S/32S)sample/(33S/32S)reference − [(34S/32S)sample/(34S/32S)reference]0.515 and Δ36S = (36S/32S)sample/(36S/32S)reference − [(34S/32S)sample/(34S/32S)reference]1.9, and the values are given in permil.
See appendix for additional discussion of experimental evidence used to assign an atmospheric origin.
Guo et al. (2009) developed a first-order kinetic model assuming that the sulfate sink is proportional to the seawater sulfate concentration. The model relies on a residence time that was derived from the present-day ~12 million year residence time of sulfate in the oceans. Their treatment therefore yielded a relaxation time for the transition equivalent to several times the modern seawater sulfate residence time. However, the residence time of sulfate in the oceanic pool most likely does not follow first-order kinetics over the range of seawater sulfate concentrations inferred for geologic time. It was most likely shorter during the GOE, and therefore the transition also would have been shorter than modeled by Guo et al. (2009). Nevertheless, the progression from mass-independent to mass-dependent relationships would have been similar.
Oxygenation likely continued during the Lomagundi carbon isotope excursion but we are concerned here about the first pervasive oxidation reflected by the transition from MIF to MDF of sulfur isotopes.
We add the cautionary note that the role of hydrothermal activity which has clearly affected other records (e.g., Isley 1995; Barley et al. 1997, 1998; Isley and Abott 1999; Condie et al. 2001) is unclear and should be carefully considered in directly tying this evidence to low level transient oxygenation and oxidative weathering of sulfide minerals. As discussed above, low-temperature hydrothermal Mo flux could have been quantitatively important under Archean anoxic conditions.
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Acknowledgments
The authors thank H. D. Holland, P. Falkowski, D. Catling, C. Reinhard, and an anonymous reviewer for constructive comments on the manuscript. The discussion of transition metal stable isotopes greatly benefited from comments and editing by S. Severmann. A. Bekker acknowledges support from an NSERC Discovery Grant. J. Farquhar acknowledges support from a NASA EXB grant and the NAI.
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Appendix
Appendix
Experimental studies of MIF and the connection to atmospheric chemical reactions
The connection between Δ33S and Δ36S values and atmospheric chemistry was explored using three different approaches. The first of these was a study by Farquhar et al. (2001), who presented results of a series of closed-cell photolysis experiments with sulfur dioxide that were undertaken with a variety of light sources. These experiments produced reaction products with large isotope variations for 33S/32S, 34S/32S, and 36S/32S, and some of these provided a qualitative match for the observations from the geologic record. This study recognized that a requirement for the photochemistry seen in these experiments is the presence of ultraviolet radiation with wavelengths shorter than ~280 nm, and that this requirement could be used as a constraint on atmospheric composition. Indeed, several key atmospheric gases absorb at these wavelengths, and this could place upper limits on their abundance. Two gases were examined in this study, ozone and carbon dioxide. By comparing the lifetime for photolysis of sulfur dioxide with its lifetime determined by physical processes (rainout and dry deposition), these workers argued that the amounts of oxygen and carbon dioxide would have to be less than ~0.01–0.002 bar (few percent of present atmospheric level) and ~0.8 bar, respectively. Further experiments are needed, however, and new findings suggest that non-atmospheric reactions may be implicated in some sulfur MIF (e.g., Watanabe et al. 2009).
The experiments by Farquhar et al. (2001) should be considered to be preliminary and it is warranted to provide a small amount of additional discussion of their possible connection to the geologic record. These experiments were undertaken with four different light sources, including two laser sources, and showed coherence between fractionations observed with light sources of similar wavelengths. This coherence was interpreted to suggest a possible dependence of the effects on the wavelength of the ultraviolet radiation. The experiments were not clear analogs of what would happen in the atmosphere and several deficiencies of the experiments are clear, namely that:
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The chemistry in the reaction cells was very complex and included effects associated with many reactions and also shielding of UV within the cells by isotopic species of the reactants and reaction products (self-shielding).
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The experiments done with laser light sources were necessarily of an unrealistically narrow wavelength band which are on the order of that of the fine structure in the absorption spectra of molecules like SO2, and are not broad enough to capture the spectral shifts due to isotope substitution (e.g., Danielache et al. 2008).
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The experiments done with more intense light sources may have included multiphoton effects—two photons absorbed by one molecule in a shorter time than it can react or relax impart more energy than a single photon and lead to a different outcome.
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The concentrations and number density of sulfur dioxide was much higher than it would be in the atmosphere, leading to the possibility of reaction pathways in the experiments that would not be relevant in the atmosphere.
In spite of these deficiencies, the experiments have been widely cited for identifying a possible candidate for the source of the effect in the Archean samples. This is because the experiments produced large magnitude isotope effects that resemble some of the features seen in the record. However, the types of isotope effects produced by the experiments may have been associated with the primary photolysis reactions, self-shielding, or with secondary reactions that occurred within the cell. These issues however remain unresolved and deserve further investigation.
The experiments of Watanabe et al. (2009) suggest it is possible for nonzero Δ33S values to be produced by abiotic reduction of sulfate mediated by amino acids, but the origin of the effect seen in these experiments is not clear, and an understanding of the origin turns out to be a critical link in making the case for relevance to the Earth’s early sulfur cycle. The experimental results do not provide a clear indication of whether these reactions also produce variations for Δ36S values by these reactions, and this has implications for the origin of the observed isotope effect. The core issue that needs to be resolved is whether the effect observed by Watanabe et al. (2009) is a kinetic isotope effect of the class referred to as magnetic isotope effects (e.g. Turro 1983; Buchachenko 1995) or whether it is a new type of kinetic isotope effect associated with weak bonding (e.g., Lasaga et al. 2008—but see Balan et al. 2009 for arguments against the existence of this type of effect).
The resolution of this issue may be related to the Δ36S values of the products of these experiments. It is not possible to rule out an effect on Δ36S values given the data, but it also is not possible to attribute it to the same step that produced the Δ33S signal observed in the experiments. It is possible that there is an effect on Δ33S values which is a magnetic isotope effect that is superimposed on other isotope effects arising from the complex reaction pathways inherent in the experiments. The latter effects would have had an impact on Δ36S values and further work is therefore needed to address this possibility.
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Farquhar, J., Zerkle, A.L. & Bekker, A. Geological constraints on the origin of oxygenic photosynthesis. Photosynth Res 107, 11–36 (2011). https://doi.org/10.1007/s11120-010-9594-0
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DOI: https://doi.org/10.1007/s11120-010-9594-0