Power, Sex, Suicide: Mitochondria and the Meaning of Life

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Power, Sex, Suicide
Mitochondria and the Meaning of Life
 
Power, Sex, Suicide

Mitochondria and the Meaning of Life

 

NICK LANE

 

 

Great Clarendon Street, Oxford
0x
2 6
DP

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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 2005

The moral rights of the author have been asserted
Database right Oxford University Press (maker)
First published 2005

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
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Oxford University Press, at the address above

You must not circulate this book in any other binding or cover
and you must impose the same condition on any acquirer

British Library Cataloguing in Publication Data

Data available

Library of Congress Cataloging in Publication Data

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Typeset by Footnote Graphics Limited
Printed in Great Britain
on acid-free paper by
Clays Ltd., St. Ives plc

ISBN 0–19–280481–2 978–0–19–280481–5

1 3 5 7 9 10 8 6 4 2

For Ana
And for Eneko
Born, appropriately enough, in
Part 6

Contents
 

List of Illustrations

Acknowledgements

Introduction Mitochondria: Clandestine Rulers of the World

Part 1 Hopeful Monster: The Origin of the Eukaryotic Cell

1. The Deepest Evolutionary Chasm

2. Quest for a Progenitor

3. The Hydrogen Hypothesis

Part 2 The Vital Force: Proton Power and the Origin of Life

4. The Meaning of Respiration

5. Proton Power

6. The Origin of Life

Part 3 Insider Deal: The Foundations of Complexity

7. Why Bacteria are Simple

8. Why Mitochondria Make Complexity Possible

Part 4 Power Laws: Size and the Ramp of Ascending Complexity

9. The Power Laws of Biology

10. The Warm-Blooded Revolution

Part 5 Murder or Suicide: The Troubled Birth of the Individual

11. Conflict in the Body

12. Foundations of the Individual

Part 6 Battle of the Sexes: Human Pre-History and the Nature of Gender

13. The Asymmetry of Sex

14. What Human Pre-history Says About the Sexes

15. Why There Are Two Sexes

Part 7 Clock of Life: Why Mitochondria Kill us in the End

16. The Mitochondrial Theory of Ageing

17. Demise of the Self-Correcting Machine

18. A Cure for Old Age?

Epilogue

Glossary

Further Reading

Index

List of Illustrations
 

1
Schematic structure of a mitochondrion, showing cristae and membranes

2
Schematic illustrations of a bacterial cell compared with a eukaryotic cell

3
Hydrogenosomes interacting with methanogens

Courtesy of Professor Bland Finlay, F.R.S., Centre for Ecology and
Hydrology, Winfrith Technology Centre, Dorset

4
Schematic showing the steps of the hydrogen hypothesis

Adapted from Martin et al. An overview of endosymbiotic models for the
origins of eukaryotes, their ATP-producing organelles (mitochondria and
hydrogenosomes) and their heterotrophic lifestyle,
Biological Chemistry
382
: 1521–1539; 2001

5
The respiratory chain, showing complexes

6
The ‘elementary particles of life’—ATPase in the mitochondrial membrane

From Gogol, E. P., Aggeler, R., Sagerman, M. & Capaldi, R. A., ‘Cryoelectron
microscopy of
Escherichia coli
F adenosine triphosphatase decorated with
monoclonal antibodies to individual subunits of the complex’.
Biochemistry
28
, (1989), 4717–4724. © (1989) American Chemical Society, reprinted with
permission

7
The respiratory chain, showing the pumping of protons

8
Primordial cells with iron-sulphur membranes

From Martin, W., and Russell, M. J., ‘On the origins of cells’,
Philosophical
Transactions of the Royal Society B
358
(2003), 59–83

9
Merezhkovskii’s inverted tree of life, showing fusion of branches

From Mereschkowsky, C., ‘Theorie der zwei Plasmaarten als Grundlage der
Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen’.
Biol. Centralbl.
30
(1910), 278–288, 289–303, 321–347, 353–367

10
Internal membranes of
Nitrosomonas
, giving it a ‘eukaryotic’ look

© Yuichi Suwa

11
The respiratory chain, showing the coding of subunits

12
Graph showing the scaling of resting metabolic rate versus body mass

From Mackenzie, D.
Science
284
: 1607; 1999, with permission

13
Mitochondrial network within a cell

From Griparic, L. & van der Bliek, A. M., ‘The many shapes of mitochondrial
membranes’.
Traffic
2
(2001), 235–244. © Munksgaard/Blackwell Publishing

14
Graph showing lifespan against body weight in birds and mammals

From Perez-Campo et al, ‘The rate of free radical production as a
determinant’,
Journal of Comparative Physiology B
168
(1998), 149–158.
By kind permission of Springer Science and Business Media

Chapter heading illustrations © Ina Schuppe Koistenen

The publishers apologize for any errors or omissions in the above list. If contacted they will be pleased to rectify these at the earliest opportunity.

Acknowledgements
 

Writing a book sometimes feels like a lonely journey into the infinite, but that is not for lack of support, at least not in my case. I am privileged to have received the help of numerous people, from academic specialists, whom I contacted out of the blue by email, to friends and family, who read chapters, or indeed the whole book, or helped sustain sanity at critical moments.

A number of specialists have read various chapters of the book and provided detailed comments and suggested revisions. Three in particular have read large parts of the manuscript, and their enthusiastic responses have kept me going through the more difficult times. Bill Martin, Professor of Botany at the Heinrich Heine University in Düsseldorf, has had some extraordinary insights into evolution that are matched only by his abounding enthusiasm. Talking with Bill is the scientific equivalent of being hit by a bus. I can only hope that I have done his ideas some justice. Frank Harold, emeritus Professor of Microbiology at Colorado State University, is a veteran of the Ox Phos wars. He was one of the first to grasp the full meaning and implications of Peter Mitchell’s chemi-osmotic hypothesis, and his own experimental and (beautifully) written contributions are well known in the field. I know of nobody who can match his insight into the spatial organization of the cell, and the limits of an overly genetic approach to biology. Last but not least, I want to thank John Hancock, Reader in Molecular Biology at the University of the West of England. John has a wonderfully wide-ranging, eclectic knowledge of biology, and his comments often took me by surprise. They made me rethink the workability of some of the ideas I put forward, and having done so to his satisfaction (I think) I am now more confident that mitochondria really do hold within them the meaning of life.

Other specialists have read chapters relating to their own field of expertise, and it is a pleasure to record my thanks. When ranging so widely over different fields, it is hard to be sure about one’s grasp of significant detail, and without their generous response to my emails, nagging doubts would still beset me. As it is, I am hopeful that the looming questions reflect not just my own ignorance, but also that of whole fields, for they are the questions that drive a scientist’s curiosity. In this regard, I want to thank: John Allen, Professor of Biochemistry, Queen Mary College, University of London; Gustavo Barja, Professor of Animal Physiology, Complutense University, Madrid; Albert Bennett, Professor of Evolutionary Physiology at the University of California, Irvine; Dr Neil Blackstone, Associate Professor of Evolutionary Biology at Northern Illinois University; Dr Martin Brand, MRC Dunn Human Nutrition Unit, Cambridge;
Dr Jim Cummins, Associate Professor of Anatomy, Murdoch University; Chris Leaver, Professor of Plant Sciences, Oxford University; Gottfried Schatz, Professor of Biochemistry, University of Basel; Aloysius Tielens, Professor of Biochemistry, University of Utrecht; Dr Jon Turney, Science Communication Group, Imperial College, London; Dr Tibor Vellai, Institute of Zoology, Fribourg University; and Alan Wright, Professor of Genetics, MRC Human Genetics Unit, Edinburgh University.

I am very grateful to Dr Michael Rodgers, formerly of OUP, who commissioned this book as one of his final acts before retiring. I am honoured that he retained an active interest in progress, and he cast his eagle eye over the first-draft manuscript, providing extremely helpful critical comments. The book is much improved as a result. In the same breath I must thank Latha Menon, Senior Commissioning Editor at OUP, who inherited the book from Michael, and invested it with her legendary enthusiasm and appreciation of detail as well as the larger picture. Many thanks too to Dr Mark Ridley at Oxford, author of
Mendel’s Demon
, who read the entire manuscript and provided invaluable comments. I can’t think of anyone better able to evaluate so many disparate aspects of evolutionary biology, with such a generous mind. I’m proud he found it a stimulating read.

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