Oxygen and the Evolution of Life . Heinz Decker l Kensal E. van Holde Oxygen and the Evolution of Life Professor Dr. Heinz Decker Kensal E. van Holde Institut fu¨r Molekulare Biophysik Distinguished Professor Emeritus Johannes Gutenberg-Universita¨t Mainz Dept of Biochemistry and Biophysics Jakob Welder Weg. 26 Oregon State University 55128 Mainz, Germany Corvallis OR 97331 [email protected] USA [email protected] ISBN 978-3-642-13178-3 e-ISBN 978-3-642-13179-0 DOI 10.1007/978-3-642-13179-0 # Springer Heidelberg Dordrecht London New York # Springer-Verlag Berlin Heidelberg 2011 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer. Violations are liable to prosecution under the German Copyright Law. The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Cover illustration: Different oxygen transport (respiratory) proteins developed after the oxygen concentration increased some billion years ago: earthworm hemoglobin (red), arthropod hemocyanin (scorpion), mollusc hemocyanin (cephalopod) (front cover, clockwise) and the myriapod hemocyanin (back cover); see also Fig. 5.8. The molecules artwork are courtesy of Ju¨rgen Markl, Institute for Zoology, Johannes Gutenberg University Mainz. Cover design: WMXDesign GmbH, Heidelberg, Germany Printed on acid-free paper Springer is part of Springer ScienceþBusiness Media (www.springer.com) Preface This book has a curious history. It evolved, like its subject, from a much simpler beginning. Both the authors have had long-standing common interests in the proteins and processes of oxygen transport in animals. During a sabbatical year that KvH spent in the laboratory of HD, our discussions broadened to encompass the much deeper question as to how oxygen transport, and indeed oxygen utiliza- tion, were related to the evolution of life. As we considered the geological and paleontological evidence, it became clear that changes in the earth’s atmosphere and biological evolution have been, and continue to be, interrelated in complex and fascinating ways. Furthermore, these relationships have important implications for human health and humanity’s future. Thus, the book grew outward from its original focus on oxygen transport, sometimes into areas in which we must confess less confidence than we would like. But, we must ask the reader’s indulgence, for we feel that the fascination of the whole story such that it is vital to try to tell it. One of us (KvH) wishes to express his thanks to the Alexander von Humboldt Foundation, whose generous support allowed the sabbatical in the Decker labora- tory. Later, both started the book at the stimulating environment of the Marine Biological Laboratory at Woods Hole where HD spent his sabbatical. Some readers may find Chapter 1 daunting, with too much dry chemistry. Skip it if you wish! Although we feel that it provides a useful background for the rest of the book, most of the following Chapters can be read intelligently without this material. We would like to thank Dr. Helmut Ko¨nig, Dr. Wolfgang Mu¨ller-Klieser, and Dr. Harald Paulsen (University of Mainz) for critical reading of several parts of the book and Christian Lozanosky for his help with the figures. We also thank Dr. Jutta Lindenborn (Springer) for all her help with the publishing process. We would like to express our thanks to our wives, Ina Decker and (the late) Barbara van Holde for their patience during the past years. Mainz, Germany Heinz Decker Corvallis, OR, USA Kensal E. van Holde v . Contents 1 Oxygen, Its Nature and Chemistry: What Is so Special About This Element? .............................................................. 1 1.1 A Brief Introduction to Oxygen ....................................... 1 1.2 Atomic Structure of Oxygen: Chemical Bonding Potential .......... 2 1.3 The Dioxygen Molecule ............................................... 5 1.4 Reactive Oxygen Species ............................................. 8 1 À* 1.4.1 Superoxide O2 ............................................... 8 1.4.2 Hydrogen peroxide (H2O2) ..................................... 9 1.4.3 Peroxyl radical (ROO*) ......................................... 9 1.5 Ozone ................................................................. 10 1.6 Water ................................................................. 12 1.7 Water Vapor in the Atmosphere ..................................... 15 1.8 Carbon Dioxide ....................................................... 15 1.9 Solubility of Gases in Water ......................................... 16 1.10 Hydrolysis and Dehydration: Central Water Reactions inBiology ........................................................... 16 1.11 Redox Reactions ...................................................... 17 References .. ................................................................ 18 2 A Brief History of Oxygen ................................................ 21 2.1 Cosmic History of the Elements ....................................... 21 2.1.1 The Sun and Solar System ...................................... 24 2.2 Formation of Earth ..................................................... 25 2.3 The Primordial Environment .......................................... 27 2.3.1 Atmosphere of the Early Earth ................................. 27 2.3.2 Water on the Earth’ Surface: The Origin of Oceans ........... 29 2.3.3 The First Greenhouse Effect .................................... 29 2.4 Life: Its Origins and Earliest Development ... ........................ 30 2.5 A Billion Years of Life Without Dioxygen: Anaerobic Metabolism ... 32 2.5.1 Some Principles of Metabolism ................................ 32 2.6 The Invention of Photosynthesis ...................................... 35 vii viii Contents 2.7 How Oxygenic Photosynthesis Remodeled the Earth ................. 38 2.7.1 The First Rise of Dioxygen ..................................... 38 2.7.2 Effects on Life: An Ecological Catastrophe? .................. 39 2.7.3 Effects on the Earth ............................................. 40 References .. ................................................................ 41 3 Coping with Oxygen ...................................................... 43 3.1 The Impact of Oxygenation on an Anaerobic World ................. 43 3.2 Production of Reactive Oxygen Species .............................. 44 3.3 Coping with Reactive Oxygen Species ................................ 47 3.3.1 Scavenger Molecules ........................................... 47 3.3.2 Enzymes for Detoxification of ROS ............................ 49 3.3.3 Antioxidant Enzyme Systems .................................. 51 3.4 How to Avoid Reactive Oxygen Species? ............................ 52 3.5 Evolving Defense Strategies ........................................... 53 3.5.1 Aggregation for Defense ........................................ 53 3.5.2 Melanin ......................................................... 54 3.5.3 Oxygen Transport Proteins Prevent Creation of Oxygen Radicals ............................................. 55 3.6 Reactive Oxygen Species as Cellular Signals . ........................ 56 3.7 Dioxygen as a Signal: Oxygen Sensor ................................ 56 3.8 Summary: Reactive Oxygen Species and Life ........................ 57 References .. ................................................................ 58 4 Aerobic Metabolism: Benefits from an Oxygenated World ........... 61 4.1 The Advantage to Being Aerobic ..................................... 61 4.2 Evolution of an Aerobic Metabolism .................................. 62 4.2.1 Special Mechanisms Needed for Aerobic Metabolism ........ 62 4.2.2 When and How Did Aerobes Arise? ... ........................ 63 4.3 Eukaryotes: The Next Step in Evolution .............................. 67 4.3.1 Distinction Between Prokaryotes and Eukaryotes ............. 67 4.3.2 The Symbiotic Hypothesis ...................................... 67 4.4 The Last Great Leap: Multicellular Organisms, “Metazoans” ........ 69 4.4.1 When, Why, and How? ......................................... 69 4.4.2 Collagen and Cholesterin ....................................... 70 4.4.3 Half a Billion Years of Stasis? ................................. 71 4.4.4 Emergence and Extinction of the Ediacaran Fauna ............ 72 4.4.5 The Bilateral Body Plan ........................................ 73 4.4.6 The “Cambrian Explosion”: Fact or Artifact? ................. 74 References .. ................................................................ 76 5 Facilitated Oxygen Transport ............................................ 79 5.1 How to Deliver Dioxygen to Animal Tissues? ...................... 79 5.2 Modes of Delivery .................................................... 80 Contents ix 5.2.1 Diffusion from the Surface .................................... 80 5.2.2 Transport via Blood as a Dissolved Gas .....................