Abstract

Photosynthesis provides energy in the Earth’s biosphere and oxygen in its atmosphere. For oxygen to be produced, two different light reactions must operate simultaneously, and in series. Known anaerobic, photosynthetic bacteria contain one or other of these photosystems, but never both. I propose that the two photosystems diverged, in structure and function, from a common ancestor, within a single, continuous, anaerobic lineage. In such cells, the two photosystems are isoenzymes encoded by orthologous genes under co-ordinated, redox regulatory control. A redox switch responds to defined environmental conditions and selects which set of genes is expressed. In these cells, the two photosystems are thus synthesised at different times. It is further proposed that the origin of oxygen-evolving photosynthesis was a simple mutation that disabled the redox switch, permitting simultaneous expression of the two sets of genes. The two, newly co-existing photosystems became connected by shared electron carriers, allowing generation of electrochemical potential high enough to oxidise water; an inexhaustible supply of reductant; and the selective advantages, and pressures, of an aerobic world.

The redox switch hypothesis predicts a specific redox regulatory control pathway in a Heteronuclear, Anoxygenic Phototroph – “HAP”. “Heteronuclear” denotes the possession of genes for both type I and type II reaction centres, a property previously thought to be restricted to oxygenic phototrophs. The predicted organism will share some of the characteristics of Chloroflexus and Oscillatoria spp. It is possible that all such lineages have died out, but this seems unlikely, since suitable habitats still exist. It is therefore to be expected that this bacterium is either undiscovered, or a known species, as yet incompletely described. “HAP” is also a good candidate for the organism that built ancient stromatolites and other microbialites in the early Archaean, up to 1 Gyr before the rise in atmospheric oxygen concentration at 2.5 to 2.6 Gyr before the present day. Elements of the redox regulatory control pathway are likely to have been conserved, and may govern the relative activities of the two light reactions in cyanobacteria and chloroplasts.

Allen JF: A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Letters 2005, 579: 963- 968.

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