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Benthic perspective on Earth's oldest evidence for oxygenic photosynthesis

Abstract : The Great Oxidation Event (GOE) is currently viewed as a protracted process during which atmospheric oxygen increased above ∼10 −5 times the present atmospheric level (PAL). This threshold represents an estimated upper limit for sulfur isotope mass-independent fractionation (S-MIF), an Archean signature of atmospheric anoxia that begins to disappear from the rock record at 2.45 Ga. However, an increasing number of papers have suggested that the timing for oxidative continental weathering, and by conventional thinking the onset of atmospheric oxygenation, was hundreds of million years earlier than previously thought despite the presence of S-MIF. We suggest that this apparent discrepancy can be resolved by the earliest oxidative-weathering reactions occurring in benthic and soil environments at profound redox disequilibrium with the atmosphere, such as biological soil crusts and freshwater microbial mats covering riverbed, lacustrine, and estuarine sediments. We calculate that oxygenic photosynthesis in these millimeter thick ecosystems provides sufficient oxidizing equivalents to mobilize sulfate and redox-sensitive trace metals from land to the oceans while the atmosphere itself remained anoxic with its attendant S-MIF signature. As continental freeboard increased significantly between 3.0 and 2.5 Ga, the chemical and isotopic signatures of benthic oxidative weathering would have become more globally significant from a mass-balance perspective. These observations help reconcile evidence for pre-GOE oxidative weathering with the history of atmospheric chemistry, and support the plausible antiquity of a terrestrial biosphere populated by cyano-bacteria well before the GOE. oxygenic photosynthesis | Great Oxidation Event | oxidative weathering | Precambrian A remarkably coherent ensemble of evidence points to a significant accumulation of atmospheric oxygen for the first time in Earth's history beginning circa (ca.) 2.45 Ga, the so-called Great Oxidation Event (GOE). In brief, this includes the disappearance of detrital pyrite, uraninite and siderite from fluvial and deltaic deposits (1), an increase in the retention of iron in paleosols (2), an enrichment of Cr and U in iron formations (3, 4), and the disappearance of sedimentary sulfur isotope mass-independent anomalies indicative of atmospheric SO 2 processing in the absence of appreciable ozone (5). These gross observations have been complemented by emerging trace element and isotopic proxies whose sensitivity to oxidative cycling now appears to extend evidence for such processes hundreds of millions of years prior. In 2.7–2.6 Gy old black shales, enrichment in Mo, Re, and Os, fractionation of Fe and Mo isotopes, and C isotope data indicating methanotrophy all suggest that O 2-rich niches already existed at that time (6–10). Stüeken et al. (11) suggested that an increase in the total S and Mo supply to marginal marine sediments at 2.8 Ga is best explained by the biological oxidation of crustal sulfide minerals. Most recently, Mo and Cr isotope compositions, as well as U enrichment data, from a banded iron formation of the Pongola Supergroup appear to reflect some partial oxygenation at ca. 3.0 Ga (12, 13). Collectively these results imply that oxidative photosynthesis had evolved hundreds of millions of years before the GOE. The superposition of pre-GOE signals for oxidative weathering with the abovementioned gross observations of a generally anoxic atmosphere represents a conundrum for which two broad and nonexclusive models have been proposed: (i) that pre-GOE oxidative weathering is the result of transient oxygenation events driven by " oxygen oases " in the marine realm (14–18); and (ii) that oxidative weathering was driven by atmospheric O 2 present at concentrations below 10 −5 present atmospheric level (PAL). Recent studies have bolstered the possibility of both operating on the pre-GEO Earth (12, 19); however, several conceptual difficulties remain. These include: the short lifetime of atmospheric O 2 as a trace gas under a reducing atmosphere (20), the strong discrepancy between oxidative dissolution and burial timescales of redox-sensitive minerals in the marine realm (21), and a general lack of Fe retention in pre-GOE paleosols that argues against sustained diffusion of atmospheric O 2 into the soil (2). We propose here an alternative model that appears to have been overlooked in many discussions of pre-GOE oxidative weathering, yet is highly attractive on mechanistic and quantitative grounds, that being intense O 2 generation—and immediate consumption—at submeter scales by benthic oxygenic photo-synthesis in the terrestrial realm, regardless of atmospheric O 2 concentrations. (Benthic is used throughout the manuscript sensu amplo to refer to microorganisms living in or attached to sediments, rocks, soils, and other natural solid substrates.)
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Stefan V. Lalonde, Kurt Konhauser. Benthic perspective on Earth's oldest evidence for oxygenic photosynthesis. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2015, 112 (4), pp.995-1000. ⟨10.1073/pnas.1415718112⟩. ⟨insu-01124400⟩



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