Palaeoproterozoic ice houses 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 (i) identifying a source of oxygen pre-dating the biological oxygen production and capable of driving the evolution of oxygen tolerance, and (ii) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically produced H(2)O(2) at the surface of the glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H(2)O(2), which interacts with seawater to produce O(2) in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H(2)O(2). Answers to the second problem are controversial and range from 3.8 to 2.2 Gyr ago. A sceptical view, based on the metals that have the 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 (less than 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 Gyr ago or above, and 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.

Figure 1

Electron activity (pϵ) of typical redox couples in water at pH 7 and 25°C (adapted from Gaidos et al. 1999). Half-reactions on the left couple spontaneously with those below them on the right, and most pairs are suitable for driving biological metabolism. The primary donor of PSII (P680) has the largest redox potential change known for any organic molecule, and in its oxidative (rest) state, it is capable of oxidizing water, producing oxygen. The thick bracket signifies the range of gases emitted from volcanic eruptions. Subaerial eruptions tend to be more oxidizing than subaqueous eruptions, so the shift in eruptive style towards subaerial vulcanism noted by Kump & Barley (2007) would have helped the eventual oxidation of the atmosphere, even though all volcanic gases are on the reducing side of the ferrous/ferric couple. Note that the term ‘oxidizing’ appears to have quite separate meanings in the geological and biological sciences. Redox couples near the quartz–fayalite–magnetite buffer in rocks are considered oxidizing by the Earth scientists, but are actually on the reducing side of the diagram and clearly faraway from the ${\text{NO}}_3^{-}$ and O₂ couples considered oxidizing by biologists.

Figure 2

The Earth's glacial history, with intervals of atmospheric anoxia indicated by the light shading (adapted from a cartoon of Lovelock 1979). Major Precambrian glaciations are indicated by ‘icicles’ dangling from a temperature versus time curve through the Earth's history, and include the Pongola of southern Africa at ca 2.9 Gyr ago, the Palaeoproterozoic glaciations between ca 2.5 and 2.22 Gyr ago (the three major units of the Huronian series in Laurentia and the Makganyene of southern Africa), the Cryogenian glaciations in the Neoproterozoic (ca 800–600 Myr ago) and the Permian and Neogene glaciations in the Phanerozoic. The UV–peroxide generating mechanism of Liang et al. (2006) is expected to operate on any ice sheet formed in an atmosphere without an ozone or other UV screen. The question mark indicates the possibility of earlier glacial intervals, not yet recognized.

Figure 3

Sterol biosynthetic pathway, with proposed modifications for anoxic operation. In eukaryotes, the oxygen-dependent steps include the conversion of squalene to squalene epoxide, and the removal of two methyl groups on the C4 carbon and one on the C14 carbon (indicated by faint circles). As indicated by the faint dotted circles, we suggest that an ancestral anaerobic eukaryote may have directly done the initial cyclization reaction on squalene rather than its epoxide, in the fashion of many bacterial squalene–hopane cyclase (SHC) enzymes that will cyclize either form. The C3 hydroxyl (if it was really there in Archaean time) could be added after the cyclization reaction as described in the text. Similarly, a variety of demethylation reactions are known from sulphate-reducing organisms that could, in principle, remove the three methyl groups from lanosterol to form ergosterol (not shown), which is the simplest sterol from which eukaryotes can grow anaerobically.

Figure 4

History of the Earth's oxygenation, showing important constraints described in the text. Adapted from Kirschvink & Weiss (2002). Question marks indicate uncertainty in the relative levels of oxygen present.