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  ‘Oxygen is the story of life on Earth. …Nick Lane’s chapters are dispatches from the frontiers of research into Earth and life history, but they contain nothing that will lose the patient reader and much that will reward.’

  Tim Radford , The Guardian

  ‘A searching analysis of the role played by free radicals in senescence… crammed with interesting information, supported by an eclectic choice of references to the recent literature… a worthy effort with a clearly argued message, full of informative and entertaining details.’

  Christian de Duve, American Scientist

  ‘Broad-ranging and densely argued … Lane’s learning and historical scope enable vivid descriptions of the role oxygen has played in determining the course of evolution … [an] ambitious and detailed work.’

  Michael Peel , Times Literary Supplement

  ‘A breathtaking, broad vision of the role of a single gas in our life, from the origin of organisms through the emergence of creatures, and to their deaths … packed full of interesting life- and death-stories… A wonderful read.’

  Peter Atkins

  ‘Lane marshals an impressive array of evidence—from the mechanics of insect flight to the levels of carbon 13 in rocks—to suggest that the ancient atmosphere may indeed have been oxygen-rich after all. But an explanation for the giant forests and creatures of the Carboniferous age is only a single part of this ambitious narrative.

  Oxygen is a piece of radical scientific polemic, nothing less than a total rethink of how life evolved between about 3.5 billion and 543 million years ago, and how that relates to the diseases we suffer from today…. This is scientific writing at its best.’

  Jerome Burne , Financial Times

  ‘Lane’s book is an extraordinary orchestration of disparate scientific disciplines, connecting the origins of life on earth with disease, age and death in human beings. In his finale, he tells us many things we ought to know about antioxidants and diet.’

  John Cornwell, Sunday Times

  ‘Enjoyable and informative… Oxygen presents an entertaining and cogent account of how oxidative stress fits in to our rapidly expanding knowledge about ageing …

  a nicely crafted account of an important element’s place in our lives … deserves to be widely read.’

  Tom Kirkwood, Nature

  ‘Nick Lane has written a meticulously detailed history of oxygen on our planet… A unifying thread of Lane’s narrative, fascinating in its irony, binds it all together: oxygen, an essential element of life, is also an agent of death.’

  Laurence A. Marschall, Natural History Magazine

  ‘informative and entertaining’

  Science

  ‘In this excellent book, Lane explains how oxygen was the cornerstone of the evolutionary explosion and reviews the theory that oxygen is implicated in ageing. He presents his theories with clarity, making them accessible to anyone with basic scientific knowledge. This is both a scholarly and readable introduction to an important topic.’

  The Good Book Guide

  ‘Enthralling… An excellent book. It held me spellbound for a 7 hour plane flight. I recommend it unreservedly.’

  Barry Halliwell, Free Radical Research

  ‘Nick Lane breaks out of the mould with a provocative discussion of oxygen’s role in evolutionary biology, age-related diseases, and the life and death of human beings... The questions he addresses are of immeasurable practical concern...

  Lane’s exhaustive research is reflected in his tight arguments and crisp prose.’

  Dan Falk, The Ottawa Citizen

  ‘Popular science writing at its very best – clear yet challenging, speculative yet rigorous. The book is a tour de force which orchestrates a seamless story out of both venerable ideas and very recent discoveries in several disparate fields.’

  Bernard Dixon

  ‘Oxygen’s history has never been told as well as Nick Lane tells it here.’

  David Payne, Focus Magazine

  OXYGEN

  Nick Lane studied biochemistry at Imperial College, University of London.

  His doctoral research, at the Royal Free Hospital, was on oxygen free-radicals and metabolic function in organ transplants. Dr Lane is an honorary senior research fellow at University College London and formerly strategic director at Adelphi Medi Cine, a medical multimedia company based in London, where he was responsible for developing interactive approaches to medical education. Articles by Nick Lane have been published in numerous international journals, including Scientific American, New Scientist, The Lancet and the British Medical Journal. He lives in London.

  Read more about Nick Lane and his writing at

  http://pages.britishlibrary.net/nick.lane

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  OXYGEN

  The molecule that made the world

  Nick Lane

  1

  1

  Great Clarendon Street, Oxford OX2 6DP

  Oxford University Press is a department of the University of Oxford.

  It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in

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  Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries

  Published in the United States

  by Oxford University Press Inc., New York

  © Nick Lane, 2002

  The moral rights of the author have been asserted

  Database right Oxford University Press (maker)

  First published 2002

  First issued in paperback 2003

  All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above

  You must not circulate this book in any other binding or cover and you must impose this same condition on any acquirer British Library Cataloguing in Publication Data

  Data available

  Library of Congress Cataloguing in Publication Data

  ISBN 0-19-860783-0

  10 9 8 7 6 5 4 3 2 1

  Printed in Great Britain by

  Clays Ltd, St Ives plc

  Contents

  1 Introduction: Elixir of Life — and Death

  1

  2 In the Beginning: The Origins and Importance of Oxygen

  16

  3 Silence of the Aeons: Three Billion Years of Microbial

  Evolution

  29

  4 Fuse to the Cambrian Explosion: Snowball Earth,

  Environmental Change and the First Animals

  54

  5 The Bolsover Dragonfly: Oxygen and the Rise of the Giants

  76

  6 Treachery in the Air: Oxygen Poisoning and X-Irradiation:

  A Mechanism in Common

  106

  7 Green Planet: Radiation and the Evolution of Photosynthesis

  131

  8 Looking for LUCA: Last Ancestor in an Age Before Oxygen

  147

  9 Portrait of a Paradox: Vitamin C and the Many Faces of an

  Antioxidant

  171

  10 The Antioxidant Machine: A Hundred and One Ways of

  Living with Oxygen

  194

  11 Sex and the
Art of Bodily Maintenance: Trade-offs in the

  Evolution of Ageing

  212

  12 Eat! Or You’ll Live Forever: The Triangle of Food, Sex and

  Longevity

  235

  13 Gender Bender: The Rate of Living and the Need for Sexes

  252

  14 Beyond Genes and Destiny: The Double-Agent Theory of

  Ageing and Disease

  283

  15 Life, Death and Oxygen: Lessons From Evolution on the

  Future of Ageing

  314

  Further Reading

  343

  Glossary

  360

  Index

  366

  For Ana

  Acknowledgements

  I am especially grateful to three people, without whom this book may never have passed from concept to reality. First, to Dr John Emsley, whose beguiling science writing and generous, enquiring mind have been an inspiration to many aspiring chemists and writers. I am grateful to John for introducing me to Oxford University Press, and for many invigorating discussions about science, society and language. Second, to Dr Michael Rodgers of OUP, whose sharp eye and masterly editorial skills have cultivated a generation of science writers. I am grateful to him for seeing potential in my first attempts to put together a story for this book, for his timely and gentle nudges towards a clear and unembellished writing style, and for his encouragement and support throughout. Finally, I thank my wife, Dr Ana Hidalgo, who has lived and breathed this book with me.

  With her wide-ranging knowledge and sure perspective, she has pointed out my foolish errors with a smile, and reinforced my conviction in the central ideas. I am chastened by her intolerance for opacity, which at times was hard to bear, but without which I fear this book would have made no sense to anyone but the author.

  I am indebted to many people who have taken the time to read and criticize parts of the manuscript with an expert eye. I am especially grateful to the academics who received an e-mail from me out of the blue, and who responded with alacrity and detailed comments. In this regard, I thank Robert Berner, Professor of Geology and Geophysics at Yale University; Donald Canfield, Professor of Ecology at the University of Southern Denmark in Odense; Dr José Castresana, in the Biocomputing Unit at the European Molecular Biology Laboratory in Heidelberg; Dr David Bremner, Reader in Applied Chemistry at the University of Abertay, Dundee; Tom Kirkwood, Professor of Biological Gerontology at the University of Newcastle; John Allen, Professor of Plant Cell Biology at the University of Lund, Sweden; and Gustavo Barja, Professor of Physiology at the Complutense University in Madrid. I am also very grateful to several colleagues for many stimulating discussions and insights: in particular Dr Barry Fuller, Reader in Surgical Sciences at the Royal Free Hospital, London;

  x • ACKNOWLEDGEMENTS

  Dr Erica Benson, Reader in Plant Biochemistry and Biotechnology at the University of Abertay, Dundee; Dr Roberto Motterlini and Dr Roberta Foresti, pioneers of haem oxygenase research at the Northwick Park Institute for Medical Research, London; and Professor Colin Green, inspiring head of the Northwick Park Institute and research dynamo.

  I also thank several friends who have read and commented on large parts of the manuscript, for giving me a better sense of what the reader might enjoy, or at least tolerate. I thank especially Vince Desmond, Ian Ambrose, Allyson Jones, Paul Asbury, Dr Malcolm Jenkins, and Mike Carter. I thank my parents and brother Max for their impassioned debates about the use of language, their willingness to engage with science from the other side of the cultural divide, and their unstinting support. Without them I would never have started.

  With all this help, one might think that few errors or infelicities could have survived. Some did, and I am lucky to have benefited from the learning and literary skills of the copy editor, Eleanor Lawrence, who has tightened and clarified the manuscript with many judicious changes.

  Finally, I thank Abbie Headon, of OUP, who has responded quickly and helpfully to my many queries about the editorial process. Any remaining faults are all my own.

  C H A P T E R O N E

  Introduction

  Elixir of Life — and Death

  Oxygen defies easy classification. Ever since it was discovered in the 1770s, its properties and chemistry have been squabbled over by scholars and charlatans alike. The controversy persists today. Oxygen is hailed as the Elixir of Life — a wonder tonic, a cure for ageing, a beauty treatment and a potent medical therapy. It is also pur-ported to be a fire hazard and a dangerous poison that will kill us in the end. The popular health press is contradictory. Inhaling pure oxygen in cosmopolitan ‘oxygen bars’ and health clinics is said to work wonders, yet the opposite — ‘high-altitude therapy’ — is claimed to eliminate superfluous oxygen, conferring the health benefits of austerity. So-called ‘active’

  oxygen treatments, meaning ozone and hydrogen peroxide, are touted as miraculous scourges of bacterial infection, or as cures for cancer; yet at the same time we are told that the secret of a long life is to eat plenty of antioxidants, to protect us against the very same ‘active’ forms of oxygen.

  Oxygen seems to attract nonsense and misinformation like a magnet.

  However muddled these accounts, they agree about one thing: oxygen is important. After all, if we stop breathing it, we will be dead in minutes.

  Our bodies are beautifully designed to deliver oxygen to each of our 15

  million million cells. All the symbolism of red blood ultimately rests in the simple chemical bonding between oxygen and haemoglobin in our red blood cells. Suffocation and drowning — the physical deprivation of

  2 • INTRODUCTION

  oxygen — are among the darkest of human fears. If we think of a planet without oxygen, we think of a sterile place pockmarked with craters, a place like the Moon or Mars. The presence of oxygen in a planetary atmosphere is the litmus test of life: water signals the potential for life, but oxygen is the sign of its fulfilment — only life can produce free oxygen in the air in any abundance. If pressed for an unemotional reason for not cutting down the rain forests or polluting the oceans, we may argue that these great resources are the ‘lungs’ of the world, ventilating the Earth with life-giving oxygen. This is not true, as we shall see, but illustrates the reverence in which we hold oxygen. Perhaps it is not entirely surprising that we seek mystical or healing properties in a colourless, odourless gas.

  This book is about life, death and oxygen: about how and why life produced and adapted to oxygen; about the evolutionary past and future of life on Earth; about energy and health, disease and death, sex and regeneration; and about ourselves. Oxygen is important in ways that most of us hardly even begin to imagine, ways that are far more fascinating than the loud claims of health features. But before we begin our journey, we need to mark out the playing field. Is oxygen an elixir or a poison, or both? And how can we tell the difference? The easiest way to find out is to go back in time, to the beginnings of our own understanding.

  Even the discovery of oxygen was controversial. Credit is usually split between the English clergyman and chemist Joseph Priestley, the Swedish apothecary Carl Scheele and the French tax-collector and father of modern chemistry Antoine Lavoisier. Scheele was first of the three, but he put too much trust in the shifting sands of aristocratic patronage and floundered without publication for six years. Priestley had no such problems. In 1774, he made oxygen by focusing sunlight onto an oxide of mercury, and was quick to write three volumes on the subject. Scheele and Priestley would have taken all the credit, except that neither grasped the full significance of the new gas. Both appreciated that burning was more vigorous in pure oxygen — Scheele even called it ‘fire-air’ — yet both thought of combustion in terms of an erroneous theory, the idea that an invisible substance known as phlogiston was released into the air during burning (rather than oxygen being taken up). They thought of oxygen as pure ‘dephlogisticated’

  air, from which all the contaminating p
hlogiston had been removed.

  Lavoisier, the chemical revolutionary and political conservative, cast off this twisted theory in the years before the French Revolution. It was

  Elixir of Life — and Death • 3

  Lavoisier who bequeathed the name oxygen, and he who finally proved that oxygen was the reactive constituent of air.1 Combustion, said Lavoisier, was the reaction of oxygen with carbon or other substances. In a famous demonstration, he showed that the Holy Roman Emperor’s diamonds (made of carbon) could be vaporized if heated in the presence of oxygen (to form carbon dioxide), but that diamonds are impervious to heat if oxygen is excluded. Diamonds are forever only in the absence of oxygen. Lavoisier went further. By collecting gases and taking precise measurements with his ultra-sensitive balances, he showed that combustion and human respiration are fundamentally the same process —

  both consume oxygen and materials containing carbon and hydrogen, to give off carbon dioxide and water.

  Lavoisier was still engaged in weighing the gases emitted by breathing and perspiration when he was interrupted by soldiers of the Revolutionary Tribunal, accompanied by an uncontrollable mob. He had made some powerful enemies, among them the revolutionary leader Jean Paul Marat. Convicted on the ludicrous charge of watering the soldiers’

  tobacco, and of appropriating revenues belonging to the state, Lavoisier was beheaded in May 1794. As the great mathematician Lagrange said, “it took but a moment to cut off that head, though a hundred years perhaps will be required to produce another like it.”

  Curiously, this famous story of the discovery of oxygen is probably wrong. Not only did the alchemists get there first, but they also had a clear appreciation of the significance of oxygen. In 1604, 170 years before Scheele, Priestley and Lavoisier, the Polish alchemist Michael Sendivogius wrote that “Man was created of the Earth, and lives by virtue of the air; for there is in the air a secret food of life… whose invisible congealed spirit is better than the whole Earth.” Sendivogius proposed that this ‘aerial food of life’ circulated between the air and earth by way of an unusual salt —

  nitre, or saltpetre.2 When heated above 336°C, nitre decomposes to release oxygen, which the alchemists knew as aerial nitre. Sendivogius 1 The name ‘oxygen’ was derived from the Greek for ‘acid-former’, in the mistaken belief that oxygen is necessary for the formation of all acids. It is necessary for some, such as sulphuric and nitric acids, but not for others, like hydrochloric acid.