Paleoproterozic Icehouses and the Evolution of Oxygen Mediating Enzymes: The Case for a Late Origin of Photosystem -- II

Abstract

Two major geological problems regarding the origin of oxygenic photosynthesis are: (1) identifying a source of oxygen predating biological oxygen production and capable of driving the evolution of oxygen tolerance, and (2) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically-produced H2O2 at the surface of glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H2O2, which interacts with seawater to produce O2 in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H2O2. Answers to the second problem are controversial and range from 3.8 to 2.2 Ga. A skeptical view, based on metals that have redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the late Archaean atmosphere (< 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date ≥2.7 Ga but could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two.

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