The First Two Billion Years

The Question

What did life on Earth do for the first two billion years of its existence?

The question seems narrow, but the answer turns out to be most of what matters. By the time the period covered in this entry ends, the air had been remade, the ozone layer had formed, the oceans had begun to clear of dissolved iron, an entirely new kind of cell had been invented, sexual reproduction was in operation, and the first organisms had begun to live in cooperative bodies of many cells working as one. None of the species a casual modern observer would recognise existed yet. There were no animals, no land plants, no macroscopic fungi. There were only microbes, in unimaginable numbers, in seawater and shallow lagoons and damp rock and the cracks of the early crust. And yet by the time microbes were finished with the planet, almost every condition required for the later world was in place.

This is the story of how a young, alien planet became Earth as we now know it.

The First Cells

By around 3.5 billion years ago, and possibly considerably earlier, the surface of Earth was already inhabited.

The earliest direct fossil evidence consists of stromatolites — layered, dome-shaped structures formed by mats of single-celled organisms, generally interpreted as the ancient equivalents of the cyanobacterial mats still found in a few protected modern environments such as Shark Bay in Western Australia ^[1]. Stromatolites of comparable form, well preserved in the rock record, appear in roughly 3.5-billion-year-old strata in the Pilbara region of Western Australia and in possibly older strata in Greenland; the biological origin of the very oldest examples remains contested at the edges, but a substantial fraction of the geochemistry community accepts them as genuine biosignatures. Earlier traces of life — chemical signatures in carbon and sulphur isotopes, rather than morphological fossils — push the appearance of microbial life back further still, to within a few hundred million years of the planet's surface becoming habitable.

What lived in those mats was a prokaryote: a single-celled organism whose DNA floats freely in the cell's interior, not enclosed in any internal compartment. Prokaryotic cells are the simplest cells we know. They have an outer membrane, a single circular chromosome, ribosomes for making proteins, the molecular machinery for energy production, and at most a few accessory structures — flagella for movement, pili for attachment, a capsule for protection. They have no nucleus. They have no organelles. They are small — typically a few micrometres across — and reproduce asexually by simple division into two daughter cells.

Modern prokaryotes are split into two great branches: the Bacteria and the Archaea. The two branches diverged extraordinarily early in the history of life, possibly very close to or even before the last universal common ancestor described in the previous entry, and have followed independent trajectories ever since. Bacteria and archaea look superficially similar under a microscope, but the molecular details of their cell membranes, their gene-expression machinery, and their characteristic enzymes show that they are deeply distinct lineages. The archaea include many of the organisms found in extreme environments — boiling vents, salt flats, the gut of cattle, the depths of the crust — and the bacteria include essentially everything else, from the cyanobacteria that fill the surface oceans to the gut microbes living in the body of any reader of this entry.

For at least the first two billion years of life on Earth, and arguably more, these were the only kinds of cells that existed. The planet was a microbial planet. There was no soil in the modern sense. There were no animals, no land plants, no macroscopic fungi, no reefs of coral, no insects — nothing a casual modern observer would recognise as a creature. The only structures of biological origin large enough to see with an unaided eye were the layered domes and mats built by single cells living together in their countless billions: stromatolites, now recognised as the oldest tangible fossils of life on Earth, and the cyanobacterial sheets from which they grew. Behind that quiet architecture, the planet was running an enormous and unwitnessed experiment in chemistry.

This was not a stalled period. It was a period of profound chemical innovation. Most of the core metabolic pathways that life on Earth still relies on today were invented by prokaryotes during this stretch. Glycolysis, the citric acid cycle, the use of ATP as the cell's energy currency, the basic decoding of the genetic message into protein, the fixation of atmospheric nitrogen, the various fermentation pathways, the family of photosynthetic systems, the chemistry of methane production: all of these were prokaryotic innovations, refined over hundreds of millions of years, and inherited largely unchanged into every later form of life. When a human cell breaks down sugar for energy, the chemistry it uses is essentially identical to the chemistry of bacteria several billion years ago. The molecular toolkit on which all later life would be built was assembled during the prokaryotic age.

The Origin Of Photosynthesis

The single most consequential prokaryotic innovation, measured by its long-term effect on the planet, was photosynthesis — the trick of capturing energy directly from sunlight and using it to drive chemistry inside the cell.

The earliest forms of photosynthesis did not produce oxygen. They were anoxygenic: they used sunlight to extract energy from compounds such as hydrogen sulphide, dissolved hydrogen, or ferrous iron in seawater, leaving sulphur or rust as waste. Anoxygenic photosynthesis is still practised today by certain green and purple bacteria living in oxygen-poor environments, and it was almost certainly the older form of the trade. It freed life from total dependence on the chemical energy already dissolved in ocean water, and it spread.

At some point — current estimates centre somewhere between roughly three billion and 2.4 billion years ago, with substantial uncertainty — a lineage of bacteria refined the photosynthetic apparatus to use a more abundant electron donor: water itself ^[2]. Splitting a water molecule (H₂O) requires more energy than splitting hydrogen sulphide (H₂S), but water is essentially limitless on a planet covered in oceans. The pay-off, for any cell that managed it, was enormous. Water-splitting photosynthesis — oxygenic photosynthesis — was a metabolic windfall, and the lineage that invented it inherited the surface ocean.

That lineage is the cyanobacteria. They are still here today; they are responsible, along with their descendants the chloroplasts of plant cells, for the great majority of the oxygen produced on Earth at every moment. From their first appearance, the cyanobacteria began to alter the chemistry of the planet, slowly at first, then irreversibly.

The Great Oxygenation Event

Splitting water has a side effect. It releases oxygen.

Free oxygen — the molecule O₂ — is highly reactive. It does not naturally accumulate in the atmosphere of a planet unless something is producing it continually. On the early Earth, the oxygen released by the first cyanobacteria did not initially build up. Instead, it reacted, on contact, with iron dissolved in the oceans and with various reducing chemicals in the seawater and atmosphere. The iron, in particular, was a vast oxygen sink: dissolved in the early oceans in enormous quantities, it bound to free oxygen as fast as the cyanobacteria could produce it, precipitating out as iron oxide — rust — and falling to the sea floor in alternating layers.

Those layers are called banded iron formations. They are preserved across great regions of the world's oldest sedimentary rocks, deposited mostly between about 3.0 and 1.8 billion years ago, with the heaviest deposition concentrated around 2.5 to 2.4 billion years ago. The rhythmic banding records, layer by layer, the slow titration of seawater iron by photosynthetic oxygen, year after year, for hundreds of millions of years. Almost all of the iron that human industry now mines from the Earth's crust — the iron that makes the steel in every building, ship, and machine of the modern era — was deposited during this period, when cyanobacteria were rusting the oceans ^[3].

Eventually the oceans ran low on dissolved iron, and the other major chemical sinks for oxygen began to saturate. With the principal sinks consumed, free oxygen began to accumulate in the atmosphere itself. The transition is recorded in the geochemistry of ancient sediments, which show a fundamental shift in the oxidation state of common elements at around 2.4 billion years ago. From then on, the atmosphere of Earth contained free oxygen, in proportions that grew slowly but irreversibly over the following billion years. This transition is now called the Great Oxygenation Event ^[3].

The consequences for early life were severe. Most of the prokaryotes alive at the time of the GOE were anaerobes — organisms for which oxygen is not just useless but actively poisonous. Free oxygen will, given the chance, react with the molecules of any cell not specifically adapted to handle it, producing reactive intermediates that damage proteins, lipids, and DNA alike. The first sustained accumulation of atmospheric oxygen was, for the existing biosphere, a slow-motion ecological catastrophe. The anaerobes were not eradicated — they survived in deep mud, in stagnant water, in the guts of later animals, and in many other anoxic refuges where they continue to live — but they were displaced from the surface of the planet by lineages that had learned to use the oxygen rather than be killed by it.

The lineages that adapted invented aerobic respiration: a way of using oxygen as the final acceptor of electrons in the breakdown of food, vastly more energy-efficient than the anaerobic alternatives. A modern aerobic cell extracts more than an order of magnitude more usable energy from a molecule of glucose than a cell relying on fermentation alone. The energetic windfall that aerobic respiration unlocked was the platform on which all later complex life would eventually be built.

A second consequence was atmospheric. Free oxygen at the top of the atmosphere is dissociated by ultraviolet sunlight and recombines into a three-atom form, ozone (O₃). With enough oxygen present, an ozone layer formed, screening out the most damaging of the sun's ultraviolet radiation. Before the ozone layer existed, sustained life on the exposed surface of the continents — even microbial life — was difficult. After the ozone layer formed, the surface of the land became, for the first time, a habitable space. The colonisation of land, when it came much later, would not have been possible without the GOE that preceded it by more than a billion years.

A third consequence was climatic. The early atmosphere had been kept warm in part by methane, a powerful greenhouse gas produced abundantly by certain prokaryotes. Free oxygen reacted with that methane, breaking it down, and Earth's surface temperature appears to have plunged in response. The roughly 2.4-billion-year-old Huronian glaciation, one of the longest and most severe ice ages in the geological record, is on the prevailing current view driven in significant part by the collapse of methane greenhouse forcing in the wake of the GOE ^[4]. Life had not just remade the chemistry of the planet's air. It had, for the first time, decisively shaped the planet's climate.

The Eukaryotic Cell

Sometime between roughly 2.0 and 1.6 billion years ago, on a planet whose air now contained measurable oxygen and whose oceans were beginning to clear of dissolved iron, a different sort of cell appeared. Molecular clock estimates place the founding event — the integration of two earlier cells into one — closer to two billion years ago, while the oldest fossils that can be confidently identified as eukaryotic consolidate around 1.6 to 1.8 billion years ago. The discrepancy is not unusual for events recorded only as molecular and morphological traces in the rock record, and a precise date may never be recoverable.

A eukaryote is a cell with internal compartments. It has a nucleus in which the DNA is gathered, mitochondria that handle energy production, and, in the lineages that gave rise to plants and many algae, chloroplasts that capture sunlight. Eukaryotic cells are typically far larger than prokaryotic ones — hundreds to thousands of times larger by volume. They reproduce by the more elaborate process of mitosis described in the previous entry, and many of them reproduce sexually, with the meiosis-and-fertilisation cycle that is a major source of the heritable variation natural selection acts upon. Every plant, animal, fungus, and protist alive on Earth today is a eukaryote. Bacteria and archaea, despite their dominance in number and in ecological reach, all remain prokaryotes.

The transition from prokaryote to eukaryote was not gradual in the usual sense. It happened by endosymbiosis — one cell taking up residence inside another, and the two becoming a single integrated organism. The previous entry mentioned this in passing as one of the events that complicates the deep tree of life. It is worth describing in full here, because everything readable above the microscope on Earth descends from the result.

The endosymbiotic theory of the origin of eukaryotic cells was proposed in detail by the biologist Lynn Margulis in 1967, in a paper published under her then-married name ^[5]. It was initially controversial; it is now overwhelmingly supported by evidence. The mitochondria inside every eukaryotic cell were once free-living bacteria, of a lineage related to the modern alpha-proteobacteria. At some point, an ancestor of all later eukaryotes — itself, on current evidence, a member of the archaea — engulfed one of these bacteria and failed, or refused, to digest it. The bacterium continued to live inside its host. Over generations, the relationship became obligate. The bacterium retained its own circular DNA — every modern mitochondrion still carries a small genome of its own, and that genome is unmistakably bacterial in character — but transferred most of its other genes to the host cell's nucleus. In return, it became the cell's energy power-plant, generating ATP at a rate no archaeal cell could match on its own. The mitochondria in the cells of any reader of these words are the direct biological descendants of the bacteria absorbed in that single ancient event.

Why did this matter so much? On the standard energetic argument, articulated most clearly in 2010 by the biochemists Nick Lane and William Martin, prokaryotic cells are constrained in size and complexity by their energy budget ^[6]. A prokaryote produces ATP across its outer membrane, and the geometry of doubling cell volume requires more than doubling the surface area available for that production. Beyond a certain size the arithmetic simply fails. Eukaryotic cells, by housing their energy-producing membranes inside numerous internal mitochondria — each itself effectively a small, dedicated power-plant — escaped this constraint. They could afford much larger genomes, much more elaborate internal architecture, and a far greater range of behaviours, because each cell could now carry hundreds or thousands of energy-producing units in parallel. The argument is debated in various details by other workers, but the broad observation — that eukaryotes are dramatically more complex than prokaryotes and that the difference traces in large part to the mitochondrial windfall — is robust.

A second endosymbiosis occurred later, in a smaller subset of eukaryotes. The ancestor of modern plants and most algae engulfed a cyanobacterium, and the cyanobacterium became the chloroplast. With chloroplasts in their cells, the plant lineage acquired oxygenic photosynthesis directly. From that moment on, photosynthesis was no longer the exclusive trade of free-living bacteria; it was carried, repackaged, into the eukaryotic world. The implications would unfold across the next billion years.

The Long Stretch

The period from roughly 1.8 billion years ago to about 0.8 billion years ago is sometimes referred to in the geochemical literature as the Boring Billion — a long stretch during which atmospheric oxygen, ocean chemistry, climate, and apparent biological diversity all seem to have changed remarkably little ^[7]. The name is somewhat misleading. It is now used by most working geochemists with the understanding that "boring" means "not punctuated by dramatic events", not "uneventful". A great deal happened during this stretch; most of it was happening at the cellular level rather than in the form of large fossils.

By the early Boring Billion, eukaryotic cells were already established. Over the following hundreds of millions of years, the major eukaryotic lineages — the ancestors of fungi, of plants and algae, of animals, of the various protist groups — diverged from one another. Sexual reproduction, with its accompanying cycle of meiosis and fertilisation, took hold in eukaryotes during this period. The oldest fossils that can be confidently identified as a sexually reproducing organism are roughly 1.05-billion-year-old red algae from arctic Canada, Bangiomorpha pubescens, recognisable from cells preserved at multiple distinct stages of a sexual life cycle ^[8]. Sexual reproduction itself is almost certainly older than that — these are the oldest fossils that demonstrate it unambiguously, not the oldest occurrences — but a billion years ago, sex was already in use.

The reasons the surface world looks "boring" during this stretch are not entirely understood and are an active research question. Atmospheric oxygen seems to have plateaued at a small fraction of its modern level — high enough to oxidise ocean surface waters but low enough that the deeper ocean remained largely anoxic and rich in dissolved sulphide. Such oceans are unfavourable habitats for many of the chemical reactions complex life depends on, and may have constrained how far eukaryotic ecosystems could expand. The plateau eventually broke, in the second half of the Neoproterozoic; that breaking, together with the climate convulsions and the explosion of complex animal life that followed, belongs to the next entry.

The First Cooperating Bodies

The remaining innovation of this period is the one that most directly links this entry to the next. Multicellularity — the construction of a single organism out of many cooperating cells — appeared, on present evidence, multiple times independently during this stretch.

The defining feature of a multicellular organism is not just that many cells are present together; cyanobacterial mats and bacterial biofilms achieve that easily. The defining feature is that the cells are clonal descendants of a single founder, that they remain in physical contact, and that the cooperation among them is sufficiently durable to count as one organism rather than as a colony of independent individuals. By that loose standard, simple multicellularity has arisen independently many times — by the most widely cited count, in at least twenty-five separate lineages, including red algae, green algae, brown algae, fungi, several protist groups, and animals ^[9]. It is not a unique evolutionary event but a recurring solution.

The fossil record for early simple multicellularity has been pushed considerably further back than was once thought. Cellularly-preserved carbonaceous fossils from the Chuanlinggou Formation in North China, recently described as Qingshania magnifica, extend the well-supported record of multicellular eukaryotes back to about 1.63 billion years ago, in the form of unbranched filaments composed of distinct cells visible under the microscope ^[10]. The slightly younger and noticeably larger decimetre-scale fossils from the 1.56-billion-year-old Gaoyuzhuang Formation, also in North China, sit alongside them in the rock record. The earlier benchmark used by an earlier generation of textbooks — Bangiomorpha pubescens, the red alga from arctic Canada dated to about 1.05 billion years ago — remains important for a different reason: it is the earliest fossil that demonstrates not only multicellularity but functionally differentiated cells, with holdfast cells anchoring the body to the substrate and reproductive cells producing spores ^[8]. That step — the move from undifferentiated filaments and clusters to bodies with internal division of labour — is the boundary between simple and complex multicellularity, and complex multicellularity in this stricter sense has arisen far fewer times than its simpler cousin: in animals, in land plants, in florideophyte red algae, in brown algae, and in a few other lineages ^[11]. Each of those originations had to solve, separately, the architectural problem of building a body from cells that do different things.

There are older candidate fossils still, more contested. A set of macroscopic structures from sediments in Gabon, dated to roughly 2.1 billion years ago — the Francevillian biota — has been interpreted by some workers as evidence of cooperative multicellular life as far back as the immediate aftermath of the Great Oxygenation Event ^[12]. The biological status of these structures remains contested, and an alternative interpretation as abiotic mineral formations has not been ruled out.

Why does multicellularity work? A loose colony of cells gains some advantages over a single cell — more efficient feeding, some protection from predation, room for division of labour — but the move from a colony to a true integrated body requires solving a particular problem: cells that cooperate are vulnerable to cells that defect. A cell that hoards resources for itself, or that reproduces independently of the body's cycle, can in principle out-multiply the cooperators and destroy the cooperative arrangement from the inside. Every multicellular organism, at every level of complexity, has had to evolve mechanisms to suppress this kind of defection — the molecular policing that keeps the cells of a body working together rather than for themselves. (Cancer, in modern animals, is an instance of that policing breaking down: a lineage of cells in a body has begun to behave as a unicellular organism again, reproducing for its own sake at the body's expense.) The early multicellular eukaryotes solved the problem in various ways — by limiting reproduction to a single specialised cell line, by ensuring development is clonal so that all body cells are genetically identical, by sequestering the reproductive cells from very early in development. The molecular detail varies among lineages; the underlying problem is the same.

By the close of the period covered in this entry — somewhere around 1.2 to 1.0 billion years ago — the planet hosted multicellular eukaryotes of several kinds alongside its much older microbial inhabitants. The cooperative bodies were mostly aquatic and unelaborate compared with what would follow, but in the form of Bangiomorpha and its contemporaries the rock record now shows the first organisms in which different cells genuinely did different things in the service of a shared body. Every plant in any later forest, every fungus in any later soil, and every animal of any size — including the species writing these words — is descended from one or another of the multicellular eukaryotes of this period.

What Follows

The first two billion years of life on Earth ended with a planet barely recognisable from the planet on which life began. The atmosphere now contained free oxygen. The ozone layer was in place. The oceans, while still chemically very different from today's, had begun the slow shift toward modern chemistry. Eukaryotic cells, complete with mitochondria and (in some lineages) chloroplasts, were established. Sexual reproduction was in full operation. Multicellularity had been invented, separately, in several lineages. The molecular and cellular foundations on which everything that comes next would be built were now in place.

What was still missing was animals in the modern sense — bodies large enough to be visible without a microscope, equipped with nerves and muscles and guts, capable of moving across the world and interacting with one another in the ways that fill the rest of this story.

The next entry takes up that part of the history, beginning with the long climate convulsions that closed the Proterozoic and the burst of new body plans that followed. From then on, life will be visible.