Bacterial Bolsheviks: PS II and the Evolution of the Oxygenic Revolution

Mathematics – Logic

Scientific paper

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0400 Biogeosciences, 1615 Biogeochemical Processes (4805), 4853 Photosynthesis, 9619 Precambrian

Scientific paper

After the rise of life itself, the most radical transformation of Earth's biogeochemical cycles was the transition from an anoxic to an oxic world. Though various studies have suggested O2 made its first bulk appearance in the atmosphere some time between 3.8 and 2.1 Ga, virtually all analyses agree the production of large quantities of free O2 was triggered by the evolution of oxygenic photosynthesis. We suggest the oldest strong geological evidence for O2 is the 2.22 Ga Kalahari Mn member of the Hotazel BIF (1), as in the oceans only free O2 can oxidize soluble Mn(II) into insoluble Mn(IV). Some have argued, however, that oxygenic cyanobacteria had originated by 2.7 Ga. The ˜500 Myr "gap" has often been interpreted as the timescale for gradual evolutionary improvement of the O2-generating system. Biochemical and genomic analyses of photosynthetic bacteria indicate that photosystems I and II, which operate together in cyanobacteria, had a long history of parallel development. Green sulfur bacteria and heliobacteria use PS-II, while green non-sulfur and purple bacteria use PS-I; none can use H2O as an electron donor. Recent genetic analyses show lateral gene transfer was rampant among photosynthetic lineages (2). Moreover, extant cyanobacteria shut down PS-II in the presence of an alternative electron donor like H2S. This suggests PS-I and PS-II came together with their functions intact. Hence, most `debugging' of the two systems predates their merger in the ancestor of modern cyanobacteria. The time interval between the lateral transfer events and the evolution of oxygenic photosynthesis could thus have been geologically short. We suggest the ˜500 Myr "gap" may result from misinterpretations. The presence of oxygenic photosynthesis is uncertain before the deposition of the Hotazel formation, in the aftermath of the Makganyene glaciation (1). A simple model of nutrient and reductant fluxes argues that, once triggered, the oxygenation of a reducing surface environment warmed by a CH4 greenhouse (3) should occur fairly rapidly, within ˜ 10 My. The trigger requires both the evolution of cyanobacteria and sufficiently high nutrient (mainly P) fluxes to allow O2 production to overwhelm reductant fluxes. P flux into the oceans in glaciated worlds correlates with increased continental weathering during glacial intervals (4). Thus, were cyanobacteria present during the Huronian glaciations, which predate 2.22 Ga (5), these glaciations should have triggered the oxygenation event. Instead, the oxygenation event seems to correlate with the Makganyene glaciation, at 2.22 Ga (6). The appearance of red beds in the Upper Timeball Hill formation directly underlying the Makganyene diamictite supports this interpretation. As would be expected from a glaciation associated with the destruction of a CH4 greenhouse, paleomagnetic data indicate the Makganyene glaciation was a global Snowball event (7). Cyanobacteria appear to have evolved in the short interval between the Huronian glaciations and the Makganyene glaciation. The lengthy delay between the earliest life on Earth and the appearance of cyanobacteria suggests that the oxygenic revolution was a fairly low probability event; planets with oxygenic biospheres may be quite rare. 1. J. L. Kirschvink et al., PNAS 97, 1400-1405 (2000). 2. J. Raymond et al., Science 298, 1616-1620 (2002). 3. A. A. Pavlov et al., JGR 105, 11981-11990 (2000). 4. K. B. F”llmi, Geology 23, 503-506 (1995). 5. S. R. Noble, P. C. Lightfoot, Can. J. Earth Sci. 29, 1424-1429 (1992). 6. D. H. Cornell et al., Precamb. Res. 79, 101-123 (1996). 7. D. A. Evans et al., Nature 386, 262-266 (1997).

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