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Oxygen: A Four Billion Year History

Oxygen: A Four Billion Year History

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Oxygen: A Four Billion Year History

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Jan 19, 2014


The remarkable scientific story of how Earth became an oxygenated planet

The air we breathe is twenty-one percent oxygen, an amount higher than on any other known world. While we may take our air for granted, Earth was not always an oxygenated planet. How did it become this way? Donald Canfield—one of the world's leading authorities on geochemistry, earth history, and the early oceans—covers this vast history, emphasizing its relationship to the evolution of life and the evolving chemistry of the Earth. Canfield guides readers through the various lines of scientific evidence, considers some of the wrong turns and dead ends along the way, and highlights the scientists and researchers who have made key discoveries in the field. Showing how Earth’s atmosphere developed over time, Oxygen takes readers on a remarkable journey through the history of the oxygenation of our planet.

Lançado em:
Jan 19, 2014

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Oxygen - Donald E. Canfield


Science Essentials

Books in the SCIENCE ESSENTIALS series bring cutting-edge science to a general audience. The series provides the foundation for a better understanding of the scientific and technical advances changing our world.

In each volume, a prominent scientist—chosen by an advisory board of National Academy of Science members—conveys in clear prose the fundamental knowledge underlying a rapidly evolving field of scientific endeavor.

The Great Brain Debate: Nature or Nurture,

by John Dowling

Memory: The Key to Consciousness,

by Richard F. Thompson and Stephen Madigan

The Faces of Terrorism: Social and Psychological Dimensions,

by Neil J. Smelser

The Mystery of the Missing Antimatter,

by Helen R. Quinn and Yossi Nir

The Long Thaw: How Humans Are Changing the Next 100,000 Years of Earth’s Climate,

by David Archer

The Medea Hypothesis: Is Life on Earth Ultimately Self-Destructive?

by Peter Ward

How to Find a Habitable Planet,

by James Kasting

The Little Book of String Theory,

by Steven S. Gubser

Enhancing Evolution: The Ethical Case for Making Better People,

by John Harris

Nature’s Compass: The Mystery of Animal Navigation,

by James L. Gould and Carol Grant Gould

Oxygen: A Four Billion Year History,

by Donald Eugene Canfield

The Cosmic Cocktail: Three Parts Dark Matter,

by Katherine Freese

Life’s Engines: How Microbes Made Earth Habitable,

by Paul G. Falkowski


A Four Billion Year History

Donald Eugene Canfield

Princeton University Press

Princeton and Oxford

Copyright © 2014 by Princeton University Press

Requests for permission to reproduce material from this work should be sent to Permissions, Princeton University Press

Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540

In the United Kingdom: Princeton University Press, 6 Oxford Street, Woodstock, Oxfordshire OX20 1TW


All Rights Reserved

Fourth printing, and first paperback printing, 2016

Paperback ISBN: 978-0-691-16836-4

The Library of Congress has cataloged the cloth edition of this book as follows:

Canfield, Donald E.

Oxygen : a four billion year history / Donald Eugene Canfield.

pages cm. — (Science essentials)

Summary: The air we breathe is twenty-one percent oxygen, an amount higher than on any other known world. While we may take our air for granted, Earth was not always an oxygenated planet. How did it become this way? Oxygen is the most current account of the history of atmospheric oxygen on Earth— Provided by publisher. ISBN 978-0-691-14502-0 (hardback)

1. Oxygen. I. Title.

QD181.O1.C36 2014

551.51'12—dc23   2013024610

British Library Cataloging-in-Publication Data is available

This book has been composed in Baskerville

Printed on acid-free paper. ∞

Printed in the United States of America

1  3  5  7  9  10  8  6  4  2


This book is dedicated to the memory of my father, Eugene David Canfield Jr., my guiding light.


I must begin by acknowledging all of my good friends and colleagues who have worked hard in various ways to help unravel the dynamics of oxygen cycling on both the modern and the ancient Earth. This book is as much their story as it is mine. You will meet most of these people as the story unfolds, but I would like to highlight the inspiration of Bob Berner, Tim Lenton, Rob Raiswell, John Hayes, Lee Kump, Penny Chisholm, Ed Delong, Nick Butterfield, Jorge Sarmiento, Osvaldo Ulloa, Bo Thamdrup, Bo Barker Jørgensen, Andrey Bekker, Bob Blankenship, Roger Buick, Fritz Widdel, Niels Peter Revsbech, Martin Brasier, Jake Waldbauer, Jochen Brochs, Birger Rasmussen, Bill Schopf, Paul Falkowski, Bill Martin, Dave Des Marais, John Waterbury, Sean Crowe, Simon Poulton, CarriAyne Jones, Jim Kasting, Minik Rosing, Christian Bjerrum, Tim Lyons, Ariel Anbar, Stefan Bengtson, Andy Knoll, Roger Summons, Dave Johnston, James Farquhar, Nick Lane, Jim Gehling, Guy Narbonne, Tais Dahl, Daniel Mills, and Emma Hammarlund. I also wish to acknowledge the constant stimulation of the NordCEE group spread between and the University of Southern Denmark, the University of Copenhagen, and the Swedish Museum of Natural History. Many of the heroes of this story are no longer with us, but their inspiration continues, and these people include Dick Holland, Vladimir Vernadsky, Preston Cloud, Karl Turekian, and Bob Garrels. This book progressed in fits and starts, but I am especially grateful to the Division of Geological and Planetary Sciences at Caltech, and especially to my host Woody Fischer for arranging a Moore Fellowship to support two months of productive bliss, together with my family and away from the distractions of home. During the course of writing, I received valuable feedback on individual chapters from Bob Blankenship, Minik Rosing, Bob Berner, Tais Dahl, Emma Hammarlund and Guy Narbonne. I am grateful to Bill Martin and to Lee Kump who provided feedback on the whole text, and especially to Raymond Cox, Tim Lyons, and my copyeditor Sheila Ann Dean, whose extensive comments and edits greatly improved the manuscript. I wish to acknowledge both the patience and extensive feedback from my editor, Alison Kalett at Princeton University Press. Images, or the data to generate them, were kindly provided by Minik Rosing, Emma Hammarlund, James Farquhar, Matt Saltzman, Niels Peter Revsbech, Ken Williford, Martin van Kranendonk, Bruce Wilkenson, Bill Schopf, Tais Dahl, Eric Condliffe, Bo Thamdrup, Jakob Zopfi, and Lawrence David. Finally, I wish to acknowledge the generous support from my funding sources including the Danish National Research Foundation (Danmarks Grundforskningsfond), the European Research Council (Oxygen Grant), and the Agouron Institute.


If you are like me, you probably don’t think a whole lot about the air you breathe unless, for some reason, it smells bad. However, our air is quite special. It contains 21% oxygen, and ours is the only world we know of (at least so far) with such elevated amounts. This is good for us because we are large animals and we need lots of oxygen to live. So also do our furry friends, cats and dogs, as well as the cows, chickens, sheep, pigs, and other animals on which we base much of our diet. Oxygen burns the fuel that heats our homes, and allows the warm glow of a campfire on a crisp autumn evening. In short, oxygen is a signature feature of Earth; the high levels in our atmosphere define the outlines of our existence, as they also generally define the nature of animal life on Earth.

Given the importance of Earth’s oxygen, we might contemplate a series of questions. So, for example, where does all this oxygen come from? Why are the levels so high? What controls the atmospheric concentrations of this important gas? We might further wonder if oxygen concentrations have always been so high and if not, how they have changed through time, and if so, why. Finally, given the importance of oxygen to the present biosphere, is there any indication that the history of atmospheric oxygen levels could be coupled in any way to the history of biological evolution on Earth?

This book is about the history of atmospheric oxygen on Earth, and I will attempt to answer these questions in the following pages. One of the inevitable conclusions, which I offer in advance, is that oxygen control is a global phenomenon, and oxygen persists in high levels because of a fascinating interplay between biological and geological processes. The nature of this interplay has changed through time, resulting in a rich history of oxygen evolution; this history, as well as we understand it, will be revealed in the pages to follow.

The story is also about the people involved in unraveling the history of oxygen evolution. Indeed, understanding this history has become a popular subject, and many scientists are now involved in its exploration. Many of these investigators are good friends and colleagues, and they have all contributed to a wonderful and rich work life. There are also heroes in this story; visionary thinkers who forged the paths down which others, including myself, follow. Some of those thinkers were decades ahead of their time.

This book is also about how we know what we know. I present the evidence. This is based, mostly, on clues left in ancient sedimentary rocks. Some of the evidence is good and some of it is not so good, especially when we look at very old rocks where the ravages of time have taken their toll. The preservation of the geologic record, however, is part of the story, and we must use the evidence that we have. This means that sometimes we are unable to draw firm conclusions. Uncertainty like this is also very much a part of the scientific process, and I therefore draw attention to it. Still, we can often look at a problem with multiple lines of evidence, and if we apply Ockham’s Razor,¹ we can usually come to a reasonable working hypothesis as to the meaning of the data. I also try to highlight instances where our ideas have evolved as the data have improved, become more abundant, or are better understood.

Not all of the evidence, however, comes from geology. There is a strong biological component to the story. We sometimes need to look at modern organisms and modern ecosystems to see how they work. They provide important clues to help us understand how the ancient world worked, especially in details that the geologic record can’t easily provide. We also must consider biological evolution. How, for example, did biological oxygen production come to be? This is a fascinating story.

Sometimes we also need to understand complex topics of, such as how photosynthesis works, or how isotopes might be used to unravel the history of oxygen. It has been my goal to make these discussions accessible to anyone interested in science, so I try to introduce difficult principles with enough background that they become broadly understandable. I also use endnotes to explain principles and processes in the detail that a specialist or an especially interested lay person might appreciate. My hope, though, is that the story does not really require one to visit the endnotes, unless the reader wants to learn even more.

Finally, this is a story about time—vast amounts of time. Planet Earth is approximately 4.5 billion years old, which is roughly one-third of the age of the universe. I studied chemistry in college, and my experience with time, at least scientifically, was limited to the hours or days of a chemical reaction. Our whole lives are but a blink of an eye in comparison to the age of Earth. Indeed, thinking about immense tracks of geologic time did not come easily to me. The enormity of geologic time challenges us to imagine how slow processes, like evolution or mountain building, can actually work. I’m now more comfortable with geologic time, and with the time scales of geological and evolutionary processes, but I sympathize with the difficulty of perceiving processes that play out over time scales immensely longer than a human life span. Anyway, the vastness of geologic time was recognized centuries ago, and made famous in the closing remarks of James Hutton’s classic 1788 book, Theory of the Earth:

The result, therefore, of our present enquiry is, that we find no vestige of a beginning,—no prospect on an end.

Not long after Hutton’s book was published, it became apparent that distinct fossil assemblages could be recognized in certain layers of rocks. This was of practical use for identifying layers that might have economic interest, but it also became obvious that these layers could be divided, subdivided, and dated relative to one another. A key principle in dating was the simple deduction, made in the seventeenth century by the Danish polymath Nicolaus Steno, that a layer of sediment deposited over another is younger than the layer below. This is known as the Law of Superposition.

Major divisions were often described based on either the loss or appearance of distinctive fossil groups, and by correlating from one outcrop to another; these divisions could be recognized from place to place and eventually around the world. Divisions were given names, and as radio-isotope dating methods became available, rocks could be dated precisely. What emerges is the geologic time scale. This is our roadmap, our measuring stick, and it is as central to geology as the periodic table is to chemistry. There are multiple scales to these divisions, ranging from eons (hundreds of millions to billions of years), to eras (tens to hundreds of millions of years), to periods (tens of millions of years), and finally to stages (millions of years). An abbreviated version of the geologic time scale is shown in figure P.1, including some key events and places discussed in the text.

Figure P.1. Geologic time scale showing major events highlighted in the text. Time scale after Gradstein (2004).

Writing this text has been both a joy and an immense learning experience. It has been great fun to try and focus my thinking on topics that have been fuzzy, and to follow the historical development of the many ideas presented here. The only negative aspect of the writing was the quick realization that I could discuss only a fraction of the relevant literature on any given subject. So I apologize in advance to my colleagues and friends whose work has gone unmentioned. It has not gone unnoticed. Despite the need to economize in the text, I hope that this book represents an up-to-date view of the subject, but I recognize that in 30 years, a very different book will likely be written. I hope you enjoy.

Don Canfield (Odense, Denmark)



What Is It about Planet Earth?

I’m sitting on the train, as I often do, traveling between Odense and Copenhagen. We’ve just pulled from the stop at Ringsted. I look out the window. The scene is typical Danish countryside of mixed farmland and forest. I pass cows grazing lazily in the field, and beyond them, a farmer is cutting hay. High above, a hawk searches for mice in the uncut grass. I love this landscape. It reminds me of the Ohio countryside where I grew up. Not spectacular, but somehow comforting and reassuring; an honest landscape not prone to bragging or trickery. I squint, and the landscape merges into a mass of green, the cows become ghosts in the distance. I open my eyes again, and we pass a small patch of dense forest (or at least what passes for forest in Denmark). My mind wanders and I reflect on what I see. Denmark is a small country and the land, including the forests, is heavily managed, so the diversity of life isn’t terribly high. You could to go the rain forests of Costa Rica or Brazil and be far more impressed with the tropical birds, frogs, insects, and the abundant greenery. Still, even in Denmark, the landscape is brilliant green and teeming with life. Indeed, no matter how you look at it, Earth is defined by abundant and diverse life. The question that preoccupies me now is why?

One might suggest that all the life we see is simply a consequence of a long history of biological evolution on Earth. In his wonderful book Life on a Young Planet, my colleague and good friend Andy Knoll from Harvard University documents the changing face of life during the first four billion years of Earth history. He shows how a variety of biological innovations, like the invention of oxygen-producing photosynthesis, for example, fundamentally shaped the history of life. After oxygen-producing organisms first evolved, other organisms that use oxygen followed, and they then prospered, multiplied, and evolved into yet other oxygen-utilizing life forms. Eventually this led to animals, the most biologically complex of all organisms on Earth. With no oxygen, there would be no animals. So, clearly, innovations during biological evolution have shaped, evened defined, the biosphere. But does evolution alone explain the bounty of life on our planet?

To consider this question, we quickly compare Earth and Mars. Scientists still hold out for the possibility of life on Mars: after all, Mars is the same age as Earth and there is some evidence for at least occasional surface and subsurface water on the planet. Even as I write, NASA’s rover Curiosity is probing the Martian surface for signs of water, and for clues as to how water interacts with the planet’s surface environment. As we will discuss more fully below, and as the tenet goes, where there is water, there may be life. Yet, if there is life on Mars, it doesn’t jump up and down like the Whos in Whoville, crying: We are here, we are here, we are here! In contrast, if intergalactic explorers probed Earth as we presently probe Mars, it would be impossible to miss Earth’s abundant life. The question is, quite simply, why is there so much life on Earth?

To answer this we will for the moment abandon considerations of evolution and start with a more fundamental question: What are the basic ingredients needed for life, at least for life as we know it? As I digest my lunch of lasagna leftovers, I proclaim that food must be important. Yes indeed, but not all organisms can eat lasagna, and I’m reminded of a whole class of creatures who don’t eat any kind of organic matter at all, but rather make their cells from simple inorganic substances. Plants fit this bill, growing from carbon dioxide and water and using the energy of the Sun to combine these compounds into cell biomass and oxygen.

Many other types of organisms also fit the bill, and most of them do not use the Sun for energy. Rather, they gain their energy from promoting the reaction between inorganic substances in so-called oxidation-reduction reactions, where electrons are transferred during the reaction. To probe this idea further, let’s think of salt. Put salt in water and it dissolves in a reaction that yields energy, but organisms cannot grow from the energy of this reaction; no electrons are transferred; and the chloride and sodium atoms have the same charge in the salt crystal as they do in the solution. Now think of cows. Cows house enormous populations of microbes in their digestive system, and many of them form methane. Many of these microbes, so-called methanogens, grow quite happily by combining hydrogen gas and carbon dioxide to form methane gas. No light is used, electrons are transferred, the methanogens are happy, and so, presumably, are the cows. Therefore, a basic necessity for life is energy, which is supplied either from light, or from a myriad of different oxidation-reduction reactions.¹ We will look at these issues in more detail in the next chapter, but for now, it’s sufficient to highlight that energy is critical for life.

Energy is critical, but we need other things too. Cells are made up of carbon, oxygen, hydrogen, nitrogen, phosphorus, and sulfur as the major ingredients, with a whole suite of trace metals and other elements as well. All of these compounds are critical in the construction of basic cellular components like the cell membrane, genetic material (DNA and RNA), and all of the proteins and other molecules used in running the cell’s machinery.

Another basic ingredient of life, at least for life as we know it, is a stable aqueous (meaning water) environment. Life likes it wet! Many organisms, of course, have evolved to live outside of the watery sphere of our planet, but they still all need water to live. So do we, but we just pack it inside our bodies. So, whether we’re talking about desert cacti, spiders, snakes, trees, or the smallest bacteria, they all need water. Indeed, this is one reason, as mentioned above, why the search for life in our solar system and beyond is tantamount to searching for liquid water. Wait, you might say, I’ve heard about small bacteria and algae living in sea ice and even in glacial ice in some cases. Very true, but if the organism is alive and growing,² it has access to liquid water. In the case of sea ice, this could be brine channels formed as salt is excluded from the growing ice; or for glaciers, high pressure induces ice melting near the bottom, providing an aqueous environment for organisms. Well then, you might add, I’ve heard that the temperature record for a living organism is about 120°C (248°F), well above the boiling point of water at Earth’s surface. True again, but these organisms are only found at high pressures, like deep in the ocean where the boiling point of water exceeds the upper temperature limit for life.

What is the big deal about water anyway? For one, water has special properties. Because of its physical structure, a water molecule is bipolar, which means that it is slightly charged with a positive charge on one side and a negative charge on the opposite side. This condition allows it to dissolve all kinds of so-called ionic chemical substances (also charged), many of which constitute the building blocks of life. These include nutrients like nitrate, ammonium, and phosphate, which form into critical components of DNA, RNA, and cell membranes, as well as a host of other substances including sulfate and a variety of trace metals, which help to build the biochemical machinery of the cell. Not only does water dissolve the substances, but these substances are also transported by diffusion and advection; and this movement provides a means by which they can be supplied to the cells. Water also provides the medium by which waste products can be exported from the cell.

The bipolar nature of water also allows for the formation of cell membranes. These separate the external environment from the inside of the cell where the business of life is conducted. Cell membranes are made up of special (phospholipid) molecules with one end containing water-loving chemical groups (hydrophilic) and the other end containing water-repelling chemical groups (hydrophobic). In

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