by Nick Lane
Over billions of years, the loss of water through the effects of ultraviolet radiation is thought to have cost Mars and Venus their oceans.4
4 The Mars Global Surveyor, which has been orbiting the red planet since April 1999, has sent back detailed pictures of sedimentary rocks that NASA scientists say probably formed in lakes and shallow seas. Erosional channels suggesting the presence of flowing water on Mars sometime in the past were described long ago, but the new images provide the first solid evidence that oceans once existed on Mars. Whether these oceans drained away under the surface of the planet or evaporated into space, or both, is as yet unknown.
26 • IN THE BEGINNING
Today, both are dry and sterile, their crusts oxidized and their atmospheres filled with carbon dioxide. Both planets oxidized slowly, and never accumulated more than a trace of free oxygen in their atmospheres.
Why did this happen on Mars and Venus, but not on Earth? The critical difference may have been the rate of oxygen formation. If oxygen is formed slowly, no faster than the rate at which new rocks, minerals and gases are exposed by weathering and volcanic acitivity, then all this oxygen will be consumed by the crust instead of accumulating in the air.
The crust will slowly oxidize, but oxygen will never accumulate in the air.
Only if oxygen is generated faster than the rate at which new rocks and minerals are exposed can it begin to accumulate in the air.
Life itself saved the Earth from the sterile fate of Mars and Venus. The injection of oxygen from photosynthesis overwhelmed the available exposed reactants in the Earth’s crust and oceans, allowing free oxygen to accumulate in the atmosphere. Once present, free oxygen stops the loss of water. The reason is that it reacts with most of the hydrogen split from water to regenerate water, so preserving the oceans on Earth. James Lovelock, father of the Gaia hypothesis and a rare scientific mind, estimates that today, with oxygen in the air, the rate of hydrogen loss to space is about 300 000 tons per year. This equates to an annual loss of nearly 3 million tons of water. Although this may sound alarming, Lovelock calculates that at this rate it would take 4.5 billion years to lose just 1 per cent of the Earth’s oceans. We can thank photosynthesis for this protection. If ever life existed on Mars or Venus, we can be sure that it never learnt the trick of photosynthesis. In a very real sense, our existence today is attributable to the early invention of photosynthesis on Earth, and the rapid injection of oxygen into the atmosphere through the action of a biological catalyst.
How life began on earth is beyond the scope of this book. Interested readers should turn to the writings of Paul Davies, Graham Cairns-Smith and Freeman Dyson, listed in Further Reading. Let us accept that life evolved in the oceans of an Earth shrouded in an atmosphere of nitrogen and carbon dioxide, but with as yet only trace amounts of oxygen. Photosynthesis probably evolved early. We will return in Chapter 7 to the theme of how and why this happened. For now, we wish to chart how life responded to the challenge of rising oxygen levels, as photosynthesis
The Origins and Importance of Oxygen • 27
Million
0
Extinction of dinosaurs
years
500
Phanerozoic
Cambrian (plants and animals)
explosion
1000
1500
Proterozoic
2000
2500
Precambrian
3000
cheanAr
3500
Origin of life on Earth?
4000
End of meteorite bombardment
Hadean
4500
Formation of the Earth
Figure 1: Geological timeline from the formation of the Earth 4.6 billion years ago to the present day. Note the immense duration of the Precambrian era. The first plants and animals appeared around the time of the Cambrian explosion 543 million years ago. The extinction of the dinosaurs was about 65 million years ago.
28 • IN THE BEGINNING
pumped out oxygen into the air and the oceans. Did oxygen pollution bring about an apocalyptic extinction, as proposed by Lynn Margulis and others, or did it stimulate evolutionary innovations? So long after the event, is there any evidence left to support either interpretation?
The gauntlet was thrown down as long ago as the 1960s by Preston Cloud, one of the pioneers of geochemistry. Even after the large techno-logical strides that the field has taken since then, his work and views still cast a long shadow today. Cloud argued that the major events of early evolution were coupled with changes in the oxygen content of the air.
Each time oxygen levels rose, life responded with exuberance. Cloud himself set three criteria to prove this hypothesis: we need to know exactly how and when the oxygen levels changed; we need to show that the adaptations of life happened at exactly the same time; and we need good biological reasons for linking the change in oxygen levels to the evolutionary adaptation. Just how far Cloud’s hypothesis is true in the light of new evidence is the focus of the next three chapters.
To make our quest more manageable, we will split Earth’s history into three unequal parts (Figure 1). First comes the Precambrian, that long and silent age before there were any visible fossils in the rocks, excepting a faltering experiment in multicellular life in the last few moments. Next comes the so-called Cambrian explosion, when multicellular life exploded into the fossil record like Athena from the head of Zeus, fully formed and wearing armour (shells in their case). Finally the Phanerozoic arrives, our
‘modern’ age of land plants, animals and fungi, when trilobites, ammon-ites, dinosaurs and mammals pursued each other in geologically swift succession. The conditions that enabled such an explosion of multicellular life were all set in the Precambrian period. We will deal with this period in Chapter 3, therefore, and with the Cambrian explosion and the Phanerozoic in Chapters 4 and 5, respectively.
C H A P T E R T H R E E
Silence of the Aeons
Three Billion Years of Microbial Evolution
It is next to impossible for us, with our historical perspective honed to decades or centuries, to conceive of the vast tract of time that ebbed away during the Precambrian era. We are dealing with a period that spanned 4 billion years — nine-tenths of the total duration of the Earth. Imagine that we are rocketing backwards through time at a rate of one millennium per second. In two seconds, we will have returned to the time of Christ, in ten seconds to the birth of agriculture; in half a minute we will see the first cave painters, and in less than two minutes we will catch a glimpse of our ape-like ancestors shuffling across the African savanna. Rushing backwards, the catastrophe that wiped out the dinosaurs will unfold before our eyes in 18 hours time; and in 4½ days we will have prime seats for the opening drama of multicellular life in the Cambrian explosion. Then we continue our journey in silence. In 44 days time, we will have returned to the first mysterious stirrings of life, and in 53 days the Earth will condense from a cloud of gas and dust.
For 40 days and 40 nights, in our compressed time scale, the Earth was populated entirely by microscopic single-celled bacteria and simple algae. With no real fossil record to bridle the imagination, it is not surprising that most of the pioneering efforts to understand the early history of life were little better than speculation. How can we have any coherent idea today of biochemical changes taking place in microbes that left little trace
30 • SILENCE OF THE AEONS
in the rocks, or of the oxygen concentration in a fleeting atmosphere long gone? The answer is indeed written in the rocks, sometimes in microscopic fossils, and sometimes in the molecular ghosts of ancient geochemical cycles. More than this, the atavistic genes of modern organisms often betray their evolutionary roots. The script written in the genes is enigmatic, although obviously meaningful. Our only guide, a molecular Rosetta stone, is the way in which the proteins encoded by the genes are used today. If a protein such as haemoglobin, the red pigment of red
blood cells, is specifically designed to bind oxygen today, and we know from genetic sequences that some bacteria also have a gene for a similar protein, there is certainly a good possibility that our common ancestor had it too. If so, we can infer that they too used the haemoglobin to bind oxygen. If, instead, they used it for something else, the clue to what that was may still be hidden in the structure of the molecule.
To understand the effect of oxygen on evolution, we need to trace two stories in the rocks and the genes: the evolution of the microbes themselves, and the timing and magnitude of the oxygen build-up in the air. Before we begin, however, we will do well to bury a hatchet in a particularly subversive double-headed ghoul. This is the common mis-apprehension that evolution necessarily tends towards greater complexity, and that microbes, being microscopic and without brains, are at the bottom of the evolutionary pile. So many evolutionary biologists have attacked the lay concept of evolution as a progression towards a higher plane, and to so little avail, that one begins to wonder whether there is a global conspiracy to thwart them. Two cautionary tales should provide a clearer perspective on Precambrian evolution. The first challenges the assumption that evolution tends towards greater complexity, while the second argues that microbes are far from simple.
In 1967, Sol Spiegelman, a molecular biologist at the University of Illinois, reported a series of experiments designed to establish the smallest unit that could evolve by natural selection. He took a simple virus that replicated itself using only a handful of genes, which consist of a string or
‘sequence’ of 4500 ‘letters’. The protein products of these genes subverted the molecular machinery of infected cells to produce new viral particles.
Spiegelman wanted to see just how simple the viral life-cycle could become if he provided the virus with all its raw materials in a test tube, instead of a host cell with its complicated molecular machinery. He gave his virus the main enzyme necessary for it to complete its life-cycle, and a free supply of all the basic building blocks needed for it to copy its genes.
Three Billion Years of Microbial Evolution • 31
The results were spectacular. For a while the virus replicated itself exactly, preserving its original gene sequence. After a period, however, a mutation caused part of one gene to be lost. Because this gene was only necessary for the virus to complete its normal life-cycle in an infected cell, and was not necessary in the test tube, the mutant virus could survive quite happily without it. More than happily, in fact: the new gene sequence was shorter than the old one, so the mutant virus could replicate itself faster than the non-mutant viruses. This faster rate of replication allowed the mutants to prevail over their competitors until they, too, were overtaken by a new mutant, an even slimmer-line virus able to replicate itself still faster. In the end, Spiegelman produced a degenerate population of tiny gene fragments, which became known as ‘Spiegelman’s monsters’. Each little monster was just 220 letters long. They could replicate at a furious speed in the test tube, but could not hope to survive in the outside world.
The moral of the tale is simple. Evolution selects for beneficial adaptations to a particular environment, and the simplest, fastest or most efficient solution will tend to win out, even if this means that excess baggage is jettisoned and organisms become less complicated. We now realize that many simple single-celled organisms, which we once thought were relics from a primitive age that had never evolved a complex lifestyle, have instead lost their ancient sophistication. We touched on fermentation in the last chapter. Far from being a simple energy-producing system that was later displaced by more efficient mechanisms involving oxygen, it seems that, as in the yeasts, fermentation is often a recent (in evolutionary terms) adaptation to oxygen-free environments, and such fermenters have actually lost their ancestors’ ability to use oxygen.
My second cautionary tale illustrates the metabolic sophistication of supposedly simple microbes. Humans and other large animals will quickly suffocate and die without oxygen, because our bulk, a community of some 15 million million cells, precludes the use of any other type of respiration.
As a result, we are rather limited in the biochemical reactions we can carry out, albeit very efficient at marshalling our limited resources. Some microbes, however, can live using oxygen to respire, but if deprived of air will simply switch to another way of satisfying their energy requirements and continue without a glitch.
The bacterium Thiosphaera pantotropha is one such, and is about as far removed as we can get from our sense of an evolutionary pinnacle: it lives on faeces. Originally isolated in 1983 from an effluent-treatment plant, it applies an extraordinary virtuosity to the extraction of energy from sewage.
32 • SILENCE OF THE AEONS
When oxygen is present, it extracts energy from a wide range of organic and inorganic substrates by aerobic respiration. When conditions become anaerobic, however, it can extract energy from thiosulphate or sulphide using nitrogen oxides instead of oxygen. The only trick missing from this metabolic cabaret is an ability to ferment. Such biochemical versatility lends the bacterium great flexibility in lifestyle — it can switch from one energy-producing process to another in response to sudden chemical changes, which are brought about by the periodic injections of dissolved oxygen used to speed up the decomposition of effluent in treatment plants.
Curiously, genetic analysis of a wide range of living organisms suggests that LUCA — the hypothetical bacterium proposed as the Last Universal Common Ancestor, the greatest grandmother of all living things in the world today — may have had a similar ability to switch between different types of metabolism, nearly 4 billion years ago. Most of her descendants appear to have lost their illustrious ancestor’s flexibility. We will return to this theme in Chapter 8.
The Precambrian, then, was a time of spectacular metabolic innovation. Microbes learnt to harness the power of the Sun, as well as the oxidizing power of oxygen, and to generate energy from an array of sulphur, nitrogen and metal compounds. The chemistry of these life-giving reactions has sometimes left subtle traces — so-called carbon or sulphur signatures — in sedimentary rocks, and occasionally, not at all subtly, in the form of billions of tons of rocks. The metabolism of ancient microbes was directly or indirectly responsible for our most important reserves of iron, manganese, uranium and gold, to say nothing of the gold prospec-tor’s false nugget, iron pyrites. These rocks and ores were not deposited continuously or synchronously, but at different times and under different environmental conditions. Their sequence has been carefully reconstructed through precise radioactive dating, and together the findings open a colourful window on oxygen and life in the formative years of our planet.
The first signs of life in rocks are found in the same Greenland rocks that we discussed in Chapter 2, and take the form of an anomaly in the proportions of different carbon isotopes they contain. This important finding was reported in the journal Nature in 1996 by a NASA-funded doctoral student, Stephen Mojzsis, and his colleagues at the Scripps Institution of Oceanography at La Jolla in California. The interpretation of
Three Billion Years of Microbial Evolution • 33
these carbon signatures in rocks is so important to our story that it is worth explaining what they are and why they are there. Not only do carbon isotopes preserve a record of the triumphs and tribulations of life, but their shifting proportions can permit surprisingly quantitative estimates of the changes in the atmospheric composition of the ancient Earth.
There are several different atomic forms of carbon (as opposed to molecular forms such as diamond or graphite). These atomic variants are called isotopes. Each carbon isotope has six protons in the nucleus, giving them all an atomic number of six. This means they are all carbon and all have exactly the same chemical properties. But the carbon isotopes differ in the number of neutrons in their nuclei and so vary in their atomic weight. The more neutrons they have, the heavier the atoms. Carbon-12, for example, has six neutrons, giving it an atomic weight of 12
(6 protons
+ 6 neutrons), whereas carbon-14 has 8 neutrons, giving it an atomic weight of 14 (6 + 8).
Carbon-12 is by far the most abundant carbon isotope on Earth (accounting for 98.89 per cent of the total) and has an honourable place in chemistry as the standard against which the relative weights of all other elements are measured. The carbon-12 nucleus is stable and does not decay. In contrast, carbon-14 is produced continuously in minute amounts (about 1 part in 1012; one part in a million million) in the upper atmosphere, through the bombardment of cosmic rays. The unstable carbon nuclei formed decay through radioactive emissions at a fixed rate.
The half-life (the time taken for half the total mass to decompose) is exactly 5570 years. This short time period (in geological terms) makes radiocarbon dating useful for determining the age and authenticity of prehistoric remains or historical documents, such as the Dead Sea scrolls and the Turin shroud.1
Fascinating as it is, carbon-14 has no further place in our story. It is the other main isotope of carbon, carbon-13, that concerns us here.
Unlike carbon-14, carbon-13 has a stable nucleus and does not decay. In this respect, it is similar to carbon-12. The total amount of carbon-13 in the Earth and its atmosphere is therefore constant (1.11 per cent of the 1 Carbon-14 is dispersed throughout the atmosphere and absorbed by living plants in photosynthesis, then eaten by animals, in proportion to its abundance in carbon dioxide. This abundance remains roughly constant because in the long term the rate of formation balances the rate of decay. When plants and animals die, however, the cessation of gas exchange or breathing means that their tissues are no longer in equilibrium with the atmosphere, so their carbon-14 content declines in proportion to the rate of radioactive decay; older organic compounds therefore contain less carbon-14.