by Nick Lane
In comparison with iron, manganese is not easily oxidized, so manganese oxide ores are unlikely to have deposited from the oceans until the dissolved iron had already been exhausted; and indeed, the Kalahari manganese field overlies a rich bed of haematite, the most highly oxidized iron ore, in the Hotazel iron formation. Such a complete deposition of iron and manganese seems to demand a surplus of oxygen. In modern waters, manganese deposition is almost invariably brought about by algal or cyanobacterial blooms, which can generate very high levels of oxygen in a short period. Considered together then, Kirschvink argues, the nutrients from the melting snowball Earth stimulated a cyanobacterial bloom, followed by a precipitate oxidation of the surface oceans, ultimately aid-ing the accumulation of free oxygen in the atmosphere.
The drama is in the speed. If the underlying rate of change is less than the buffering capacity of the environment to absorb that change, the system as a whole can maintain a pernicious chemical equilibrium.
The tendency to approach a stable equilibrium is antithetical to life, which might almost be defined as a state of dynamic disequilibrium. In Chapter 2, we saw that the Earth was saved from the sterile fate of Mars by
Three Billion Years of Microbial Evolution • 49
an injection of oxygen from photosynthesis into the atmosphere, preventing the oceans from ebbing away into space with the loss of hydrogen gas. After this, however, the world sank into a second period of stasis, in which the oxygen produced by cyanobacteria was balanced by the uptake from bacterial respiration, and reaction with rocks, dissolved minerals and gases. This new equilibrium lasted from about 3.5 billion years ago until 2.3 billion years ago, nearly a quarter of the Earth’s history.
Life on Earth was saved from an interminable ecological balance between iron-loving bacteria, stromatolites and cyanobacteria by the sudden punctuation of the snowball Earth, a shock that rocked it from slumber-ing complacency with a second big injection of oxygen.
The history of the next billion years lends support to this view of life: not a lot happened, at least to the naked eye. After the deposition of the vast banded iron formations, the dramatic climate swings, the tectonic movements, the oxidation of the surface oceans and the rusting of the continents, Earth seems to have settled down once more to a period of equilibrium, in which a new balance was established. If isotope ratios and fossil soils are to be believed, oxygen levels remained more or less constant at 5 to 18 per cent of present atmospheric levels throughout this period — more than enough for oxygen metabolism to become widespread among our ancestral eukaryotic cells. Better oxygenation would also have increased the concentration of sulphate, nitrate and phosphate in the oceans, lifting these particular brakes on growth. We begin to see simple multicellular algae in the fossil record, and a better preservation of a wider range of eukaryotic cells, suggesting that there may have been a blossoming of genetic variety.
The evolutionary success of our eukaryotic ancestors may well have been linked directly with the higher oxygen levels. We shall see in Chapter 8 that eukaryotes are a hotchpotch of different components.
Each individual cell is crammed with hundreds or even thousands of tiny organs, known as organelles, which carry out specialized tasks such as respiration or photosynthesis. Modern life would be unthinkable without these organelles, yet they are aliens within. Some of them show signs of independent origins. One type, called mitochondria, evolved from a strain of purple bacteria. They are the sites at which the oxygen-requiring steps of respiration are carried out in all eukaryotic cells, including those of
50 • SILENCE OF THE AEONS
plants and algae. Photosynthesis in plant and algal cells takes place in another organelle — the chloroplast — which is derived from cyanobacteria.
Eukaryotic cells are thought to have developed from their primitive precursors into a kind of internal marketplace during the long period of environmental stability beginning around 2 billion years ago. Small bacteria were engulfed by the primitive eukaryotic cells, but somehow survived inside the larger cells like Jonah in the whale. As a result, the eukaryotes eventually became a community of cells within cells.4 The stalemate must have encouraged the trading of metabolic wares in exchange for shelter. This intimate symbiotic relationship was ultimately so successful that the internalized bacteria are now barely recognizable as once-independent entities. The long-term success of the relationship, however, conceals an interesting paradox. Let us take the mitochondria as an example.
Imagine: 2 billion years ago a small purple bacterium was engulfed by a larger cell, which then had a case of indigestion. Whether the larger cell was predatory, or the invading cell infective, is immaterial. The fact that the insider deal persisted at all means that it was never seriously detrimental. The fact that it finally dominated, to the extent that virtually all eukaryotes have mitochondria, means that it must ultimately have been beneficial. The advantage is obvious in today’s world: mitochondria use oxygen to generate energy, by far the most efficient means of biological energy generation known. In those days, though, it ought to have been a different matter. The problem is as follows. The energy currency of all cells is a compound called ATP (adenosine triphosphate). Cells use ATP
either directly or indirectly to power most of the metabolic reactions that maintain life and make new material for the cell to grow. Both the symbiotic bacteria and their hosts would have produced ATP independently, by fermentation in the case of the eukaryotes, and by burning carbohydrate ‘fuel’ using oxygen in the case of the bacteria. The bacterial method was much more efficient, so they could produce much more ATP.
Like all currencies, ATP is exchangeable. Any ATP produced by the bacteria could in principle be consumed by the host. For the host to benefit in this way, though, the bacteria would have had to export ATP to the 4 There is some dispute about whether the eukaryotes were produced in a single fusion event between different types of bacteria, or whether a series of engulfments took place. With the exception of chloroplasts, evidence is beginning to favour a single event, or concentrated series of events, which occurred before the deepest evolutionary branches of the eukaryotes.
Three Billion Years of Microbial Evolution • 51
host cell. Modern mitochondria have pores in their bounding membranes that enable this to happen; but free-living bacteria do not have an ATP
export mechanism. On the contrary, free-living bacteria are protected by membranes and cell walls specifically designed to keep the outside world out and the inside world in. Genetic studies indicate that the ATP-export mechanism in mitochondria evolved later, albeit before the major evolutionary branches of the eukaryotes. But if the hosts could gain no extra energy from their guests, how did they benefit? Why did this symbiosis flourish?
Evidence from similar symbiotic relationships today suggests that, while the host cell may have gained no energetic benefit, it might instead have been protected from within by its oxygen-guzzling guests. By converting oxygen to water, the symbiotic bacteria would have protected their hosts from potentially toxic oxygen. This acquired immunity to oxygen poisoning would have enabled the early eukaryotes to inhabit the shallow waters where oxygen levels were highest, and so exploit the benefits of light — either by photosynthesis in the case of algae, or by grazing off the freshest pickings in the case of consumers. Over time, the success of this early pact would have encouraged an even closer union, in which the host cell spoon-fed its guests with nutrients, and they in return exported ATP into the cell.
The idea that cells might protect themselves against oxygen by associating with other cells is borne out at a looser level, which may have had even more profound consequences in the long run. When modern oxygen-hating eukaryotes such as the ciliate protozoa are placed in oxygenated water, their first impulse is to swim away to water with less oxygen. The more oxygen there is, the faster they swim. But what if there is no escape? When their surroundings are equally well oxygenated and flight is futile, the ciliates institute plan B:
they clump together in a mass.
Even anaerobic cells have some capacity to consume oxygen. When cells clump together in this way, each cell benefits from the oxygen consumption of its neighbours. Other communally living cells also seem to have benefited from spreading the burden in this way. For example, stromatolites, those great domed communities of cyanobacteria, are known to have contained many other types of cells, including anaerobic bacteria.
Only the top few millimetres of most stromatolites are composed of oxygen-producing cyanobacteria, whereas the deeper levels are home to billions of anaerobic cells, despite high oxygen levels during the daylight hours. Again, each cell benefits from sharing the oxygen load.
52 • SILENCE OF THE AEONS
Rising oxygen levels may therefore have favoured confederations of cells, from which grew the most efficient energy system for powering life
— numerous mitochondria per cell5 — and the first stirrings of multicellular organization. If so, it is quite possible that a tendency to huddle together as clumps of cells, to alleviate the toxicity of oxygen, was an impetus to the evolution of multicellular life. Certainly, it is a fact that all true multicellular organisms contain mitochondria. Of the thousand or so simple eukaryotes that lack mitochondria, not one is multicellular. People are thus confederates of cells and of cells within cells. We shall see in Chapter 8 that the design of the human body actually restricts oxygen delivery to individual cells: multicellular organization still serves the same purpose in us that it did for our single-celled ancestors.
The Precambrian is drawing to an end. We have travelled down 3 billion years. There has been little to see but much has changed. Without these changes, the explosion of multicellular life that is soon to follow would have been impossible. I have argued that the changes were linked with rises in atmospheric oxygen.
In summary: the first signs of life, the carbon signatures in the rocks of western Greenland, date back to 3.85 billion years ago. By 3.5 billion years ago we find microscopic fossils, resembling modern cyanobacteria, and large stromatolites. If appearances are not deceptive, these cyanobacteria were already producing oxygen. However, it is not until nearly a billion years later, 2.7 billion years ago, that we have the first definitive evidence of cyanobacteria, as well as the first signs of our own ancestors, the eukaryotes, in the form of tell-tale biochemical fingerprints in the rocks. These eukaryotes made sterols for their membranes, a task that requires oxygen. From the activity of sulphate-reducing bacteria we know that oxygen levels rose at this time, perhaps to around 1 per cent of present atmospheric levels. Another 500 million years later, 2.2 billion years ago, oxygen levels rose again, following hard on the heels of the snowball Earth. In the period of geological unrest that followed, huge banded iron formations precipitated from the oceans all around the world. Free oxygen was probably needed for the genesis of at least some of 5 Just as a car might be 100 horse-power, so a eukaryotic cell with 100 mitochondria could be said to be 100 bacteria-power.
Three Billion Years of Microbial Evolution • 53
these formations. At the same time, around 2.1 billion years ago, we see the earliest fossils of eukaryotes. By 2 billion years ago, we have rock-hard evidence of oxygen accumulating in the air: fossil soils, continental red-beds and uranium reactors. Oxygen levels reached around 5 to 18 per cent of present atmospheric concentration. In the rocks, we see a sudden explosion of diversity in fossil eukaryotes. Many have mitochondria. All the elements of the modern world, bar true multicellular organisms, are in place.
Then little changed. For a billion years, oxygen levels remained steady at 5 to 18 per cent of present atmospheric levels. The prolonged period of tranquillity saw a number of quiet developments in the history of life — the flourishing of the eukaryotes, genetic diversification, colonization of new habitats, and, in the shape of the algae, the first tentative steps towards multicellular life. And yet: in the face of all these quiet advances, nothing more complicated than a few slimy green tendrils evolved in the course of a billion years. None of this prepares us for what happens next. In a geological blink of an eye, 543 million years ago, the whole of creation as we know it exploded into being. Whatever happened?
C H A P T E R F O U R
Fuse to the Cambrian Explosion
Snowball Earth, Environmental Change and the
First Animals
The cambrian explosion — the eruption of multicellular life at the beginning of the Cambrian era — has taxed the finest minds in biology ever since Darwin himself. Why did it happen so suddenly?
Did it really happen so suddenly? Darwin had assumed that natural selection should be a process of gradual, cumulative change, and was troubled by the abrupt appearance of fossilized animals in the rocks of the Cambrian era. He hoped, as many have since, that the Cambrian explosion would turn out to be an aberration of the fossil record. If this were the case, then the discovery of older fossils would one day prove that the Cambrian animals had evolved slowly after all — that there had, in reality, been a long Precambrian fuse to the Cambrian explosion. This position was not unreasonable, as most Cambrian fossils known at the time were hard calcified shells, with few remnants of the soft animals that once lived inside; small wonder then that the soft bodies of their unprotected predecessors had perished without fossil record. Perhaps the Cambrian explosion recorded no more than the evolution of shells.
The Burgess shale put paid to the idea that life had only invented shells at the beginning of the Cambrian. Discovered high in the Canadian Rockies by Charles Doolittle Walcott of the Smithsonian Institution in the early years of the twentieth century, this mid-Cambrian shale contains such an astonishing variety and preservation of soft body parts that
Snowball Earth, Environmental Change and the First Animals • 55
it has acquired almost iconic status. Many of the fossils examined by Walcott were ‘shoehorned’, to borrow the late evolutionary biologist Stephen Jay Gould’s phrase, into modern taxonomic groups. The story of their reclassification by Harry Whittington, Derek Briggs and Simon Conway Morris of Cambridge University, was the subject of Gould’s book Wonderful Life, published in 1989. Under bright lights and operating microscopes, the Cambridge team reconstructed the anatomy of numerous strange bilaterally symmetrical creatures, placing one ‘weird wonder’
after another into taxonomic groups of their own. Their names spoke for themselves: Hallucigenia, Anomalocaris, Odontogriphus — each referred to creatures that seemed to correspond to nothing alive today; stalk-eyed, armour-plated, shutter-jawed monstrosities more reminiscent of cartoon Martians than sensible Earthly animals.
In celebrating their strangeness, Gould dwelt on both the sudden appearance of this wealth of biological variety and its eclipse over subsequent geological time. No fundamental body plans have been added to the collection that had evolved by the end of the Cambrian (all insects, for example, have three body segments and six legs), and many variants that existed then have since disappeared without trace. Then, ungratefully soon after Gould had published Wonderful Life, two well-preserved fossil beds from the same period were discovered in Greenland and China, and the strangeness of the Cambrian fauna came to be seen in a more conventional light. Some of the weird wonders turned out to have been interpreted upside down, or to have had the parts of other animals mistakenly grafted onto them. Conway Morris, now one of the world’s leading authorities on Cambrian biology, has remarked that the real marvel is how familiar so many of these animals seem. The deep similarities between many of the Cambrian animals were first proved statistically in 1989, by Richard Fortey of the Natural History Museum, London and Derek Briggs, then at the University of Bristol, and have since been confirmed by other workers.1 But if the strange variety of Cambrian fauna is no longer contentious, the roots of the explosion are still fiercely debated.
The question remains surprisingly similar to that which troubled Darwin: was the Cambrian explosion really a sudden event, or had there been a slow-burning
fuse stretching back into the Precambrian?
1 Their approach is known as cladistics. Essentially, rather than seeking differences, cladistic analyses enumerate the fundamental similarities between different species to draw a web of inter-relatedness.
56 • FUSE TO THE CAMBRIAN EXPLOSION
We do have more to go on than did Darwin — a century of searching late Precambrian rocks for signs of life has duly turned up a few examples.
The most famous are the so-called Ediacaran fauna, a group of radially symmetrical animals, along the lines of jellyfish: pads and pillows of amorphous protoplasm. Some reached a considerable size, measuring a metre [3 feet] or so across. Originally named after their place of discovery, the Ediacara Hills in Australia, similar fossils have since cropped up across all six continents, and date to the Vendian period, 25 million years before the Cambrian. Their discovery, however, did not so much dispel the enigma of the Cambrian as deepen it. Dolf Seilacher, a German palaeobiologist now at Yale University, claims that these stuffed bags of protoplasm, the gentle vegan Vendobionts (as he affectionately calls them), were far from being the ancestors of the bilaterally symmetrical, armour-plated Cambrian animals, but were instead a doomed early experiment in multicellular life that either fell extinct before the beginning of the Cambrian period or got eaten by the shutter-jawed Cambrian predators.
While Seilacher’s view has been vigorously contested by many palaeontologists, who claim that at least some Vendobionts survived into the Cambrian, few dispute that these strange floating bags do not fit comfortably into modern taxonomic groups.
But the Vendobionts were not the only inhabitants of the Vendian period. Small worms (perhaps several centimetres [an inch or so] in length) burrowed through the mud of the sea floor. Their tracks are preserved, amazingly, in the sandstones of Namibia and elsewhere. These signs of animal movement in the bottom sediments are the first in the long course of the Precambrian, and from then on, similar tracks were left throughout the modern age. The worms live on and leave them still today.