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Before many millions of years had passed, some cells had learned to use sunlight to split water. Rocks formed over 3,000 million years ago show that the atmosphere contained traces of oxygen by then. Photosynthesis had begun.

Photosynthesis opened an evolutionary door. Without an oxygen-rich atmosphere there could have been no animals. Most of the prokaryotes, protists and fungi alive today could never have evolved without photosynthesis; they too depend on oxygen. But oxygen is lethal to all living matter unless protective devices are installed. Every oxygen-breathing or oxygen-tolerant species in the world is equipped with molecules designed to destroy deadly oxygen derivatives. The first organisms ever to develop photosynthesis, presumably primitive cyanobacteria, must have been able to detoxify the oxygen they generated. Otherwise, photosynthesis would have been suicide.

This simple deduction raises further questions. How did the earliest organisms detoxify oxygen? Perhaps they used a simple combination of amino acids, such as those associated nowadays with marine bioluminescence28. Alternatively, a copper or iron containing enzyme might have been used, as in most present-day terrestrial organisms. Whatever the mechanism, it must have evolved before photosynthesis, or at latest simultaneously with it; so why did it evolve before there was any apparent need for it? Perhaps, to begin with, the mechanism served some entirely different purpose. Or perhaps it did not pre-exist, but arose as a by-product when the prototype chlorophyll was synthesised. Could a single anabolic process have given rise to both a chlorophyll-like and a coelenterazine-like28 molecule, creating photosynthesis and oxygen-protection in one fell swoop? The questions remain.

Did all early-Earth organisms develop the equipment to detoxify oxygen? Three scenarios can be imagined.

1. Most organisms alive at the time could detoxify oxygen; photosynthesis emerged in a pre-prepared world. But if so, why? This takes us

28 Amino acids are the building blocks of proteins. Amino acid is to protein as a single popper bead is to a necklace. A dietary requirement for most bioluminescent organisms today is a molecule called coelenterazine, which is made from three amino acids joined together. Coelenterazine penetrates into cells and reacts very quickly with oxygen, emitting a brief flash of light when it does so. Perhaps the original function of coelenterazine was to protect against oxygen toxicity. It is an essential part of the diet of many marine organisms today, not only luminescent ones (though bioluminescence is very widespread in marine life), but its source remains mysterious. No one knows what species makes it, or why.

back to the previous questions. Why would an oxygen-detoxifying mechanism have evolved in a world without oxygen? What function could it have served before there was any anything to detoxify? And what was it?

  1. There were no other organisms. There was only one "species" (the photosynthetic one), or a very few closely related types. Therefore, life was presumably very localised and thinly spread. The early Earth ecosystem was seriously lacking in diversity, which means it was unstable. Therefore life had only a tenuous hold on the planet and was always likely to die out. Since life obviously survived, this scenario seems unlikely.
  2. All other organisms were wiped out by the deadly new pollutant, oxygen, except for a few that survived in oxygen-free enclaves just as anaerobic organisms do today. This is the likeliest scenario. Photosynthesis unleashed a mass extinction 3,000 million years before the earliest one known from the fossil record. Perhaps this is why all extant organisms seem to have derived from a single common ancestor. There might have been several different origins of life, but only one lineage survived after oxygen appeared in the atmosphere.

Are we limited to these three scenarios? The atmosphere's oxygen content climbed only very slowly from its initial zero value. It took the better part of 2,000 million years to reach its present level. When photosynthesis first began, the resulting oxygen level was so minute that even a rudimentary protection mechanism would have sufficed. So protection against oxygen poisoning might have evolved slowly and gradually. Nevertheless, photosynthesis must have forced a separation between oxygen-tolerant organisms, later to become bacteria and eukaryotes, and oxygen-intolerant ones, later to become archaea. Yet Woese and his colleagues date the separation of the archaea from the bacteria and "eukarya" to two thousand million years ago, not three. Why did atmospheric oxygen take a thousand million years to force this separation? No one has the answer.

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