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Oxygen and the Evolution of Life . Heinz Decker l Kensal E. van Holde Oxygen and the Evolution of Life Professor Dr. Heinz Decker Institut fu ¨ r Molekulare Biophysik Johannes Gutenberg-Universita ¨ t Mainz Jakob Welder Weg. 26 55128 Mainz, Germany hdecker@uni-mainz.de Kensal E. van Holde Distinguished Professor Emeritus Dept of Biochemistry and Biophysics Oregon State University Corvallis OR 97331 USA vanholde@asbmb.org 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 encompas s the much deeper question as to how oxygen transport, and inde ed oxygen utiliza- tion, were related to the evolution of life. As we considered the geological and paleontological evidence, it became cle ar 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 1.4.1 Superoxide 1 O 2 À* 8 1.4.2 Hydrogen peroxide (H 2 O 2 ) 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 Hydrolys is and D ehydr ation: Central Water R eactions in Biology 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 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 Def ense 53 3.5.2 Melanin 54 3.5.3 Oxygen Trans port 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 Ediacara n 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 viii Contents 5.2.1 Diffusion from the Surface 80 5.2.2 Transport via Blood as a Dissolved Gas 81 5.2.3 Oxygen Trans port Proteins: What They Must Do? 82 5.3 Modes of Dioxygen Binding to Oxygen Transport Proteins 84 5.3.1 Cooperative and Noncooperative Binding 84 5.3.2 How Does Cooperativity Work?: Models for Alloste ry 86 5.3.3 Self-Assembly and Nesting 88 5.3.4 Why Complex Multisubunit Oxygen Transport Proteins? 89 5.4 Modulation of Dioxygen Delivery by Oxygen Transport Proteins: Heteroallostery 89 5.4.1 Modulation by the Products of Anaerobic Metabolism: the Bohr Effect 90 5.4.2 The Haldane Effect 90 5.4.3 The Root Effect 91 5.4.4 Temperature Dependence 92 5.4.5 Evolutionary Aspects of Regulation . . . 93 5.5 Diversity of Oxygen Transport Proteins 93 5.5.1 Hemogl obins 94 5.5.2 Hemer ythrins 96 5.5.3 Hemocyanins 96 5.6 Evolution of Oxygen Transport Proteins 99 5.7 Was Snowball Earth a Possible Trigger for OPT Evolution? 101 5.8 From What Proteins Did Oxygen Transport Proteins Evolve? 102 5.9 Oxygen Transport Proteins and “Intelligent Design” 103 References . . 103 6 Climate Over the Ages; Is the Environment Stable? 107 6.1 Climat e and Glaciations in Earth’s History . 108 6.1.1 The First Massive Glaciat ions; the Huronion Event: A Role for Methane? 108 6.1.2 Later Proterozoic Glaciations 110 6.1.3 Phanerozoic Climate and Glaciations . . 111 6.2 How Did Life Survive Glaciations? 116 6.3 Milestones of Life in the Phanerozoic 118 6.4 Inorganic Cycling of Carbon Dioxide 121 6.5 Is Our Environment Stable? 122 6.6 Recent Global Warming 124 References . . 124 7 Global Warming: Human Intervention in World Climate 127 7.1 Recent Climate Cha nges 127 7.2 Physical Consequences of Global Warming . . 129 7.2.1 Shrinking Ice and Glaciers 129 7.2.2 Sea Level Changes 130 7.2.3 Changes in Ocean Currents 131 Contents ix 7.2.4 Local Climate and Weather 132 7.2.5 The Danger of Methane Releases 133 7.2.6 Greenhouse to Icehouse and Vice Versa? 133 7.3 Human Consequences of Global Warming 134 7.3.1 Direc t Consequences of CO 2 and Temperature Increase 134 7.3.2 Sea Level Rise 135 7.3.3 Extreme Weather 136 7.3.4 Effects on Agriculture 137 7.4 Control of Global Warming 138 7.4.1 Positive and Negative Natural Feedback Mechanism 138 7.4.2 Human Effects to Control Global Warming 139 7.4.3 The Long View 139 References . . 140 8 Oxygen in Medicine 143 8.1 Hypoxia 143 8.1.1 High-Altitude Hypoxia 144 8.1.2 Hypoxia Arising from Medical Cond itions 145 8.2 Oxidative Stre ss 145 8.2.1 Nature of Oxidative Stress 145 8.2.2 Special Examples of Medical Consequences of Oxidative Stress 146 8.3 Treatment of Oxidative Stress 149 8.4 Beneficial Roles of ROS 150 8.4.1 SCN and Primary Immune Response 150 8.4.2 Nitric Oxide 151 References . . 153 9 Oxygen and the Exploration of the Uni verse 157 9.1 What Is Essential for the Development of Life as We Know It? 157 9.2 What Makes O 2 Necessary for Complex Life on Habitable Planets? 158 9.3 Seeking Evidence for Extraterrestrial Life 158 9.4 Life in the Solar System? 161 9.4.1 Terrestrial Planets 161 9.4.2 Icy Moons 163 9.5 Oxygen Supply Problems in Extraterrestrial Voyages 164 9.6 Problems Facing Exten ded Extraterrestrial Settlement or Colonizaton 166 9.6.1 Adjusting the Planetary Envir onment: Terraforming 166 9.6.2 Adjusting the Organism: Biofo rming 167 References . . 168 Index 169 x Contents [...]... negative logarithm of the concentration of protons: pH ¼ À log ½Hþ Š: Thus, the higher the pH value, the lower the proton concentration and therefore the degree of dissociation of water This behavior of water depends strongly on the temperature, the higher the temperature the lower the pH Since many organisms adapt their body temperature to that of their environments, the pH value of the body will also... roles in the evolution of life on Earth A great deal of the Earth’s oxygen is contained in water About 70% of Earth’s surface is covered by water and these oceans have long served as the major habitat of life Organisms themselves consist of between 60 and 95% of water Thus, water is fundamental to life Water has particular and unusual properties due to the special electronic structure of the water... core, the nucleus The number of protons in a nucleus gives its atomic number and its positive charge Add the number of neutrons and you have the atomic mass The nucleus of the most common isotope of oxygen contains eight protons and eight neutrons, and thus has an atomic number of 8, and 16 atomic mass units It is designated in conventional shorthand as 16O There exist other isotopes (mainly 17 O and. .. 1.4 Reactive Oxygen Species A number of reactive oxygen derivatives can result from the reaction of the singlet and triplet states of dioxygen with themselves or with other compounds Only a handful of these are of importance in living systems Their chemical properties and generations are briefly introduced here; their biological significance will be considered in detail in Chap 3, and some of their medical... bonds of oxygen are quite stable, and much of Earth’s chemistry is explained by this fact For example, the abundance and stability of the silicates such as quartz, that make up much of the Earth’s crust depends on the strength of the covalent Si–O bond and the vast amount of water depends on the O–H bonds Oxygen can form covalent bonds with a number of elements, but exceptionally important for life. .. Th, and 40K) produce heat in the interior of the Earth The kinetic energy of captured planetesimals would further contribute to the heating of the surface of Earth as they collided with it A planetesimal with a speed of about 11 km sÀ1 would deliver the same amount of energy as the same mass of TNT (trinitrotoluene) However, these sources would not alone explain the melting process According to the. .. electrons in the remaining two sp3 orbitals will still strongly attract protons on other molecules (see Fig 1.2b) These hydrogen bonds play a major role in forming the structures of proteins, nucleic acids, and water (see below) All of these properties of oxygen are an inevitable consequence of the physical laws of our universe and the subatomic structure of the oxygen atom As we shall see in Chap 2, the existence... of oxygen atoms is in turn a necessary result of the evolution of the universe 1.3 The Dioxygen Molecule Virtually all of the oxygen in the air we breathe is present as the diatomic molecule O2 which is correctly called dioxygen This is an extremely stable molecule, in which the atoms are held together by very strong covalent bonding In elementary chemistry, covalent bonding is described in terms of. .. as gluons, leptons, and quarks from which all other particles can be made, at a temperature of about 1027 K After 10À6 s (1 ms), the infant universe had further expanded and cooled to about 1012 K and the basic particles of matter – neutrons, protons, and electrons – had formed from the elementary particles Thus, very early, H Decker and K.E van Holde, Oxygen and the Evolution of Life, DOI 10.1007/978-3-642-13179-0_2,... happened to these gases? It is generally accepted that in the early stages of Earth formation the solar wind and heat of the sun blew away much of the light gases such as hydrogen, helium, methane and ammonia (see Seki et al 2001) This is also true for much of the water vapor which could not condense on the hot Earth Thus, mainly silicates and other minerals were retained and the actual atmosphere of the early . Oxygen and the Evolution of Life . Heinz Decker l Kensal E. van Holde Oxygen and the Evolution of Life Professor Dr. Heinz Decker Institut. p. 2, the existence of oxygen atoms is in turn a necessary result of the evolution of the universe. 1.3 The Dioxygen Molecule Virtually all of the oxygen

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