Nick Lane - Power, Sex, Suicide: Mitochondria and the Meaning of Life

Power, Sex, Suicide

Mitochondria and the Meaning of Life

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Power, Sex, Suicide

Mitochondria and the

Meaning of Life

N I C K L A N E

Great Clarendon Street, Oxford ox2 6dp

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Nick Lane 2005

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First published 2005

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ISBN 0192804812 9780192804815

1 3 5 7 9 10 8 6 4 2

For Ana

And for Eneko

Born, appropriately enough, in Part 6

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Contents

viii Contents

Schematic structure of a mitochondrion, showing cristae and membranes

Schematic illustrations of a bacterial cell compared with a eukaryotic cell

Hydrogenosomes interacting with methanogens

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

Schematic showing the steps of the hydrogen hypothesis 58

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 : 15211539; 2001

The respiratory chain, showing complexes

The elementary particles of lifeATPase 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 , (1989), 47174724. (1989) American Chemical Society, reprinted with permission

The respiratory chain, showing the pumping of protons 87

Primordial cells with iron-sulphur membranes

From Martin, W., and Russell, M. J., On the origins of cells, PhilosophicalTransactions of the Royal Society B (2003), 5983

Merezhkovskiis inverted tree of life, showing fusion of branches 112

From Mereschkowsky, C., Theorie der zwei Plasmaarten als Grundlage der Symbiogenesis, einer neuen Lehre von der Entstehung der Organismen.

Biol. Centralbl. (1910), 278288, 289303, 321347, 353367

Internal membranes of Nitrosomonas, giving it a eukaryotic look 128

Yuichi Suwa

The respiratory chain, showing the coding of subunits 144

Graph showing the scaling of resting metabolic rate versus body mass 160

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

x List of Illustrations

Mitochondrial network within a cell

From Griparic, L. & van der Bliek, A. M., The many shapes of mitochondrial membranes. Traffic (2001), 235244. Munksgaard/Blackwell Publishing Graph showing lifespan against body weight in birds and mammals 271

From Perez-Campo et al, The rate of free radical production as a determinant, Journal of Comparative Physiology B (1998), 149158.

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.

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 Dsseldorf, 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 Mitchells chemiosmotic 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 won-derfully 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 ones 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 scientists 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;

xii Acknowledgements

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.