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A Matter of Life and Death

Christian de Duve

Oxygen: The Molecule that Made the World. Nick Lane. x + 374 pp. Oxford University Press, 2002. $35.

It is generally believed that life originated in an oxygen-free environment and remained strictly anaerobic for more than one billion years, until cyanobacteria started splitting water with the help of sunlight, causing free oxygen to appear in the atmosphere for the first time. According to a widely accepted theory, this event brought about the extermination of most living forms, which were victims of the lethal effects of the gas (as a strict anaerobe would be today). By chance, a few rare organisms escaped this "oxygen holocaust" by acquiring in time the necessary protective mechanisms. Eventually some descendants of these organisms gained the ability to use oxygen as an electron acceptor in reactions coupled to the assembly of adenosine triphosphate, turning simple detoxification into what was to become the highest form of biological energy retrieval. This development finally gave rise, by way of advanced aerobic bacteria, to the mitochondria that power the vast majority of eukaryotic (nucleated) cells today.

This story is wrong, Nick Lane tells us in Oxygen, and is unsupported by any solid evidence. Not that he disputes the toxicity of oxygen; on the contrary, most of his book deals with this property. What he questions is the occurrence of an oxygen holocaust and the premise of this hypothetical catastrophe. Our young planet always contained small amounts of oxygen, he informs us, as a result of the photochemical dissociation of water by ultraviolet light and loss of hydrogen to outer space. Life always had to deal with oxygen toxicity and developed adequate protections at a very early stage. It entered the oxygen age smoothly, long prepared for its onslaughts.

Lane, a science writer with a doctorate in biochemistry, argues his point forcefully, with the support of a number of references. Readers who, like myself, have taken the "oxygen holocaust" scenario more or less for granted will gain much from this part of the book, although they will perhaps wish more space had been allowed to the defenders of the disputed theory. Many will probably also learn with interest that the oxygen content of the atmosphere has varied considerably with time as a result of factors such as climatic changes and organic carbon burial, leading to strange effects on, for example, the body size of animals.

Early life, however, occupies only part of Oxygen. Soon the author, jumping over three billion years of evolution, turns to the present and to his main interest—free radicals, their biological effects and their neutralization by antioxidants. Discussing "a hundred and one ways of living with oxygen," he takes us on an instructive tour of a number of timely topics, including protection against radiation, the fight against cancer, dietary fads and what he calls the "triangle of food, sex and longevity." The last chapters are devoted to a searching analysis of the role played by free radicals in senescence, ending with the conclusion that "oxygen is not just the engine of evolution and life, but also the single most important cause of ageing and age-related disease."

The book is crammed with interesting information, supported by an eclectic choice of references to the recent literature. Its title is misleading, however, because little is said about the beneficial effects of oxygen or the main functions that depend on its use, including respiration, oxygen transport, electron transfer, protonmotive force and oxidative phosphorylation. More surprisingly, there is no mention of peroxisomes, typical membrane-bounded organelles of eukaryotic cells within which a number of hydrogen peroxide–producing oxidases are enclosed together with catalase, which breaks down hydrogen peroxide to water and oxygen—a very suggestive association.

Unfortunately, the book contains more than a few troubling lapses, even within Lane's own field of specialization. For example, we are told that "the chemical energy derived from the split [of water] is used to bind carbon dioxide from the air and package it into the sugars, fats, proteins and nucleic acids that make up organic matter." As the author very well knows, energy is not derived from the splitting of water but, on the contrary, is needed for it. Twice, the biological discrimination in favor of the lighter isotopes of carbon and sulfur is incorrectly ascribed to easier breaking of their bonds with oxygen rather than to faster kinetics. In a footnote, a stick insect's resemblance to a stick is attributed to "convergent" evolution, neglecting the fact that it takes two to converge; what Lane means to allude to is mimetism. Hemophilia and color blindness are said to result from mutations in the Y chromosome, whereas they are actually attributable to mutations in the male's single X chromosome. Also, Lane tends to use misleadingly teleological language: For example, he refers to molecules evolving "for a purpose" and says that "plants produce toxins to safeguard them against being eaten."

Even more distracting is Lane's frequent recourse to a ponderous and probably useless imagery, an attempt, no doubt, to convey material that demands a fair degree of chemical sophistication to a more general readership. It is doubtful that many readers will derive enlightenment from being told that Hox genes "behave like opinionated newspaper proprietors, who influence the tone or coverage of their papers on particular issues," that iron is restrained in the core of a protein "in the manner of a horse wearing blinkers," or that lipid-attacking hydroxyl radicals "become mired in the lipid like a rugby player who got the ball but couldn't escape the scrum." Nor are many likely to better understand the mechanism of a free radical–initiated chain reaction by learning that the free radical "leaves the reactant short of an electron, just as a mugger leaves the victim short of a handbag" and that the resulting formation of another radical is "as if having your handbag snatched deranges your mind and turns you into a mugger yourself, restless until you have snatched someone else's bag," with all ending well when "two radicals react with each other, and their unpaired electrons conjoin in blissful chemical union; or when the free radical product is so feebly reactive that the chain reaction fizzles out, like handbag thieves overcome with remorse."

In conclusion, this book is a worthy effort with a clearly argued message, full of informative and entertaining details. But it leaves too much out to quite measure up to its title, and it could, with more careful editing, have avoided a number of unfortunate scientific and stylistic blemishes.

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