It will be the life and death of you

September 12, 2003

Imagine the scene in 1621: King James I of England stands on the banks of the River Thames, with thousands of his subjects, watching the maiden voyage of the world's first submarine. Over the course of three hours, the wooden craft is rowed the ten miles from Westminster to Greenwich. The spectators become curious about how the air is being refreshed for the 12 oarsmen. Eyewitness accounts say that the inventor of the device that made the voyage possible, Cornelius Drebbel, used a bottle of "liquor" to refresh the "vital" parts of the air. That "liquor" was most likely oxygen, generated in Drebbel's alchemical laboratory by heating nitre (potassium nitrate). It was another century and a half before Carl Scheele and Joseph Priestley published their discoveries of the gas and Antoine Lavoisier named it oxygine .

This remarkable tale sets the tone of a book that repeatedly challenges received wisdom and textbook assumptions. Nick Lane's central point in Oxygen: The Molecule that Made the World is that oxygen is a two-faced molecule. Although we suffocate in minutes without it, all the time we are breathing oxygen its highly reactive chemical progeny (known as "free radicals") are damaging our cells and ageing us.

Lane has written a wonderful book about this dual role of oxygen in life and death. He sheds light on these human preoccupations by tracing the co-evolution of life and atmospheric oxygen on planet earth. This is a scientific saga as compelling as any creation myth and Lane tells it with appropriate zeal.

The story begins 4 billion years ago in a world without oxygen. The atmosphere is not the Jupiter-like concoction of hydrogen, methane and ammonia we once thought it was, but a duller mixture of carbon dioxide and nitrogen with less than one molecule in a million of oxygen. This tiny fraction is the product of ultraviolet sunlight splitting water. By 3.5 billion years ago, life has emerged, and the modest generation of oxidants by sunlight is triggering a crucial evolutionary step. Reconstructions of the Last Universal Common Ancestor (Luca) reveal that early life evolved some capacity to metabolise oxygen and defend against its highly reactive free radical by-products, before it evolved the capacity to produce oxygen.

This solves one of the great chicken-or-egg puzzles in biology: that the colourfully named cyanobacteria that first acquired the trick of liberating free oxygen in photosynthesis, sometime before 2.7 billion years ago, evolved in its absence.

So how could they have acquired any defences against the potentially fatal oxidants they liberated? The answer used to be that they poisoned themselves and the rest of the oxygen-hating biosphere in an oxygen holocaust, which triggered the evolution of anti-oxidant defences. Now we know some of those defences were already in place. Instead of an oxygen holocaust, life would have flourished as bacteria acquired the means to use oxygen for respiration in the most energy-yielding reaction available to life. A winning combination was born.

Paradoxically, the world had to wait half a billion years before the "great oxidation" of the atmosphere 2.2 billion to 2 billion years ago. Even after that rise, oxygen comprised only 1 to 2 per cent of the atmosphere, but it was enough to facilitate the evolution of a new kind of aerobic life: the eukaryotes (cells in which the genetic material is contained in a nucleus).

Or so the story goes. It could be that eukaryotes evolved in local oxygen oases before the great oxidation or that they did not appear until long after. We really do not know yet. But we can be sure that the evolution of eukaryotes was a difficult step. So too was the evolution of sex that came with them, and Lane makes a fascinating case that we may have oxygen to thank for that.

Remarkably little happened for over a billion years after the great oxidation despite the fact that there was sufficient oxygen to fuel the metabolism of multicellular eukaryotes. The first fossils that look like multicellular algae are 1.6 billion years old but appearances can be deceptive. Small marine animals appeared by 800 million years ago, and by packaging organic material into fast-sinking faecal pellets they may have played a role in a second rise of oxygen in the earth's atmosphere about 800 million to 550 million years ago. This interval of earth history (the Neo-Proterozoic) was also a time of repeated extreme glaciations of the planet (the so-called snowball earth events). Oxygen appears to have been rising before, between and after these glaciations, but must have dropped during them, as biological productivity was greatly suppressed on the frozen planet.

By the end of the glaciations there was enough oxygen in the atmosphere (perhaps 10 per cent) to allow the evolution of larger animals with hard shells that could be well preserved in the fossil record. They burst on to the scene in the Cambrian explosion about 540 million years ago.

With the rise of land plants from about 400 million years ago, and their flourishing in the coal swamps of the Carboniferous 300 million years ago, oxygen was driven up again. Giant dragonflies the size of seagulls flew through the Late Carboniferous forests while millipedes over 1m long trundled along the ground. It has long been speculated that such gigantism reflects a past atmosphere more oxygen rich than the present concentration of 21 per cent, with some researchers estimating 35 per cent. The problem with this scenario is that increases in the oxygen content of the air increase the ease with which forest fires can be started and the ferocity with which they burn. Not to mention the extra anti-oxidant defences that life would have required.

The evolutionary saga sets the context for understanding the impact of oxygen in our own bodies. Lane explains the role of oxygen in ageing, why Dolly the cloned sheep aged prematurely, and what we can learn from the remarkable longevity (given their metabolic rate) of birds and bats.

Most telling is the fact that the concentration of oxygen where it is used in our cells (by the mitochondria that were once free-living bacteria) is orders of magnitude lower than in the atmosphere we breathe. That alone should caution us against spending too much time in oxygen bars or sleeping in an oxygen tent. As Paracelsus taught, the poison is the dose. Lane also applies this wisdom to the consumption of vitamin C as an anti-oxidant "therapy". The final prognosis is that oxygen sets a maximum human lifespan of about 130 years, and there is little we can do about it.

Throughout the book, Lane revels in the creative process of scientific discovery. He clearly wants more young people to dream of becoming scientists, and he writes in a way that will captivate them as well as his scientific colleagues.

There are many specific points on which I disagree with him, but to dwell on them would be to miss the wider point of the book. Lane understands that science thrives on such debate, but that scientists also need to move beyond the narrow confines of our specialist fields in order to tackle wider questions. Lane's synthesis is both broad and in depth, and that is exactly the kind of science and science writing we need.

Tim Lenton is an earth system modeller, Centre for Ecology and Hydrology, Natural Environmental Research Council, Edinburgh.

Oxygen: The Molecule that Made the World

Author - Nick Lane
ISBN - 0 19 850803 4 and 860783 0
Publisher - Oxford University Press
Price - £20.00 and £8.99
Pages - 374

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