Oxygen made us. But what made oxygen, asks Nick Lane Life’s a gas

XYGEN is life. That’s true not just for us: rocks, crushed by the weight of sediment and all animals and plants need oxygen to time. With ardour, patience and skill, they can O unleash the energy they scavenge from be marshalled into a convincing story. their environment. Take away oxygen and William Schopf had those qualities. Two organisms cannot produce enough energy to decades ago he thought he had the story, too. support an active lifestyle, or even make them A palaeontologist at the University of California, worth eating. Predation, an essential driver of Los Angeles, he was investigating the Apex evolutionary change, becomes impossible. cherts of Western Australia, 3.5-billion-year- It is easy to picture a planet without oxygen. old rocks that are among the oldest on Earth. It looks like Mars. Our nearest planetary In 1993, he announced that they contained neighbour was probably once a water world 11 different types of “microfossil” that looked too, primed for life to evolve. But it lacked a for all the world like modern photosynthesising vital ingredient: a protective shield of ozone cyanobacteria (Science, vol 260, p 640). derived from oxygen. Without an ozone layer, The finding fitted a global pattern. Other the sun’s rays slowly atomised the Martian 3.5-billion-year-old Australian rocks contained water. The hydrogen floated off into space rippling structures that looked like fossil while the oxygen oxidised the iron-rich stromatolites. A few examples of these Martian topsoil, turning it rust-red. Perhaps structures, domed edifices up to a metre high there is – or was – life on Mars. But if so it never built by cyanobacteria, still eek out a marginal progressed beyond the bacterial stage. existence in salty lagoons on the coast of So how did Earth get lucky? Ten years ago, Western Australia and elsewhere. Meanwhile, when I was writing my book Oxygen, it didn’t 3.8-billion-year-old rocks from Greenland seem too big a deal. Photosynthesising had reduced levels of one of the two stable bacteria were the magic ingredient. These tiny carbon isotopes, carbon-13, compared with organisms popped up in Earth’s oceans early the other, carbon-12 – a chemical signature on, sometime between 4 and 3 billion years of photosynthesis. It seemed that life had ago. In the couple of billion years that come early to Earth: astonishingly soon after followed, their oxygenic exhaust fumes slowly our planet formed some 4.6 billion years ago, did the job. By 600 million years ago, the air photosynthesising bacteria were widespread. was primed for complex animal and plant life. This emerging consensus lasted only until Now this cosy story has collapsed. We are no 2002, when palaeontologist Martin Brasier of longer so sure how Earth’s atmosphere got – the University of Oxford unleashed a barrage and retained – its oxygen-rich atmosphere. of criticisms. The Apex cherts, he claimed, “Photosynthesis by itself was not enough,” were far from being the tranquil sedimentary says Graham Shields, a geochemist at basin evoked by Schopf. In fact, they were shot University College London. “It was a complex through with hydrothermal veins that were no dance between geology and biology.” setting for cyanobacteria. Other evidence that Uncovering life’s earliest origins is never the rocks had undergone convulsions in the an easy task. There are no large animal or past made the rippling stromatolites no more plant fossils to draw on: these only make biological in origin than ripples on a sandy an appearance starting around 600 million beach. As for the microfossils Schopf had years ago. Yet perhaps remarkably, hints of identified, they ranged from the “almost

life’s humble beginnings do survive in ancient plausible to the completely ridiculous”. > andrew hen

36 | NewScientist | 6 February 2010 6 February 2010 | NewScientist | 37 ”With all of oxygen’s ups and downs, life on Earth was Did lichens help oxygen to finally break free? even luckier than we thought to get as far as it has”

This very public spat produced no clear Our best guess is still that cyanobacteria shows that, by 1.9 billion years ago, levels of outcome, but since then new evidence has were around some time before this event. breathable oxygen in Earth’s atmosphere were been emerging. In 2006, Thomas McCollom Persuasive evidence is converging on a date back down to the merest trace. of the University of Colorado in Boulder and around 2.7 billion years ago (see diagram, We don’t know why. It might have been a Jeffrey Seewald of the Woods Hole right). Research from Linda Godfrey and knock-on effect from a big freeze: if Earth did Oceanographic Institution in Massachusetts Paul Falkowski of Rutgers University in New indeed enter a snowball phase, glaciers would found that reactions known as Fischer- Brunswick, New Jersey, indicates that the have scoured huge amounts of nutrients from Tropsch syntheses can occur in hydrothermal modern nitrogen cycle kicked off around this the underlying rock. When the ice eventually vents, leaving a carbon isotope signature that time. This requires free oxygen to form nitrogen retreated, melted by the build-up of volcanic mimics photosynthesis with no need for a oxides, suggesting that a first whiff of oxygen – greenhouse gases in the atmosphere, those Y RAR biological explanation. The mere possibility not even 1 per cent of today’s levels – had just nutrients would have found their way into the OTO LIB

that hot water might have massaged the appeared (Nature Geoscience, vol 2, p 725). oceans. One idea is that they nourished a huge H E P evidence in Australia and elsewhere was That squares with evidence from Robert Frei transient bloom of cyanobacteria that quickly C EN

damning enough for the duo. “The possibility of the University of Copenhagen, Denmark, died and rotted, in the process consuming all /SCI E C

Mind the gap must be entertained that complex life was not and his colleagues that the oxidative the oxygen they had once produced. EN present on Earth, or at least not widespread, weathering of rocks kicked off around this time E OF SCI Y

If, as seems increasingly likely, photosynthesising until a much later date,” they wrote (Earth too. They measured levels of chromium in E cyanobacteria first made an appearance in Earth’s and Planetary Science Letters, vol 243, p 74). ancient marine rock layers known as banded Stinking oceans oceans around 2.7 billion years ago, why did they That conclusion was supported by a iron formations. Exposed to oxygen in the air, Oxygen levels in the atmosphere soon cyanobacteria did produce the first oxygen Earth’s anoxic stasis was broken in the take so long to make a difference to Earth’s air? reanalysis of “biomarkers” found in the metal is weathered from rocks and washed recovered again as rates of photosynthesis and in Earth’s atmosphere, all the evidence is they end by a dramatic series of snowball Earths, One possibility is that the oxygen’s first 2.7-billion-year-old Australian shales. These out to sea, where it reacts immediately with weathering established a new equilibrium, at lacked the oomph to push levels much above indicating bursts of oxygen, beginning about chemical mission was to oxidise all the iron and organic molecules had been thought to iron, settles to the ocean bottom and forms about 10 per cent of present-day levels. But 10 per cent of present levels in the long term. 750 million years ago and recurring over the compounds like hydrogen sulphide in the oceans. indicate the presence of cyanobacteria, but in these layers. The chromium signature in them this was no fresh dawn of a high-octane world: That has led William Martin, an expert in following 100 million years. They broke the Only after it had done that was it free to escape 2008 an Australian team concluded that the suggests there was essentially no oxidative quite the reverse. This time, the oxidative cell evolution at the University of Düsseldorf eternal loop: soon afterwards, oxygen levels into the atmosphere. shales had been contaminated by ancient oil weathering before 2.7 billion years ago, after weathering of sulphides on land filled the in Germany, and others, to come up with a shot up and never looked back. Animal life Perhaps the most persuasive answer, that had filtered down into the sediments which chromium became significantly more oceans with sulphate. That in turn fuelled a controversial theory: that the boring billion soon exploded onto the scene. though, is purely geological. It comes from some time after the rocks first formed (Nature, mobile (Nature, vol 461, p 250). hardy group of bacteria that filled the oceans was anything but boring. In fact, the stinking What made the difference this time? One veteran geologist Heinrich Holland of Harvard vol 455, p 1101). Even more damningly, in If these coordinated changes are the calling with sewer gas – hydrogen sulphide – turning oceans were the true cradle of life. Evidence intriguing possibility is that it was down to the University. He points the finger at gases such September 2009 a French team discovered cards of the first photosynthesising bacteria, them into stinking, stagnant waters almost behind this idea includes the fact that organisms that had evolved in a leisurely way as methane and hydrogen sulphide that are living bacteria buried deep down in ancient there is still a mysterious hiatus of 300 million entirely devoid of oxygen, rather like the mitochondria, the powerhouses of all during the boring billion: terrestrial red and constantly spouted out by volcanoes. They rocks of a similar age (PLoS One, vol 4, p e5298). years before the great surge in oxygen 2.4 billion deeper levels of the Black Sea today. It was the complex, oxygen-respiring “eukaryotic” cells green algae and the first lichens. “I suspect would have reacted with the first free oxygen years ago. The gap is less embarrassing than a herald of an extraordinary stasis in Earth’s today, were once far more varied, sometimes the final big rise in oxygen was caused by to form carbon dioxide and sulphur dioxides, billion years, but still needs explaining (see environment lasting nearly a quarter of its “breathing” sulphur or nitrogen instead of the greening of the continents from around effectively removing the oxygen from Crumbling edifice “Mind the gap”, left). Yet this puzzle masks a history – a period dubbed the “boring billion”. oxygen, or even emitting hydrogen gas. It 800 million years ago,” says Shields. Terrestrial circulation (Geochimica et Cosmochimica Perhaps the decisive blow came in August more fundamental new twist to the tale. But hang on: what happened to the seems that these mitochondria originated algae and lichens get their nourishment in Acta, vol 73, p 5241). last year, when Daniele Pinti of the University It is that the great oxygenation event was oxygenic utopia in which life supposedly grew in the stinking oceans of the boring billion, part by breaking down the rocks on which they Holland proposed that two processes took of Quebec in Montreal, Canada, and his perhaps not as decisive an event as we thought. and prospered, evolving the complex cells that which were full of the chemical imbalances live. These nutrients flooded into the oceans, place over geological time. First, the supply of colleagues announced results from a survey It certainly happened – a suite of geochemical went on to make up animal and plant life? The that power life today in places, like deep-sea stimulating more and more photosynthesis radioactive fuels in Earth’s interior gradually of the Apex cherts using advanced microscopy evidence leaves little room for doubt on that answer is that it probably never existed. If hydrothermal vents. by both cyanobacteria and the more advanced dwindled, reducing its internal temperature. techniques. They concluded that the rocks had score – and it was traumatic, too. Evidence algae that had evolved in the meantime. That in turn damped down the rate of volcanic formed in a hydrothermal vent at a searing of a sudden drop in ultraviolet radiation It did not all end in a “bloom and a bust” this emissions, and the rate at which oxygen- 250 °C or more – way too hot for cyanobacteria. penetrating to Earth’s surface 2.4 billion years O on the up time because lichens kept right on eating away consuming gases entered the atmosphere The “microfossils”, they said, were mostly ago indicates it was enough to create the ozone O2 on the up at the rocks. They sustained a higher rate of The rise of oxygen in Earth’s atmosphere has experienced many setbacks since the gradually fell too. deposits of iron oxides and clay minerals layer – a pivotal event that ensured our The rise of oxygen in Earth’s atmosphere has experienced many setbacks since the erosion, and constant flow of nutrients into first photosynthesising cyanobacteria appeared, probably 2.7 billion years ago Second, the volcanic gases themselves (Nature Geoscience, vol 2, p 640). planet’s history diverged from that of Mars. the ocean, even after the scouring glaciers of Steep final rise in contained more oxygen. Oxygen produced by the These new lines of evidence mean that the It also seems to have been the forerunner oxygen to today’s level various snowball Earth phases had melted. first cyanobacteria would have steadily oxidised oldest undisputed signs of cyanobacteria are to a “snowball Earth”. If Joe Kirschvink of the Life’s story on Earth is a complex one, Volcanic hydrogen sulphide and Oxygen level down surface rocks. As those rocks cycle through the now fossils found in rocks from the Belcher California Institute of Technology in Pasadena Volcanic hydrogen sulphide and Oxygen level down perhaps more complex that we ever methane keep oxygen down to almost zero again Earth’s mantle through the standard processes Islands in northern Canada dating from just and many others are correct, the oxygen imagined. After many false starts, a singular 2.7-2.4 bya 1.9 bya of subduction and convection, rocks with an extra 2.1 billion years ago. So where does that leave produced by cyanobacteria oxidised the combination of chemistry, biology and SNOWBALL load of oxygen gradually fed through to the gases our ideas about how life evolved, and the part potent greenhouse gas methane, precipitating 10 geology finally came together to unleash the EARTH “BORING BILLION” emitted by volcanoes. oxygen played in that evolution? 8 a global freeze. “That raises the spectre of one 8 Terrestrial algae oxygen we breathe. Even then, many ups and (”greening of As cyanobacteria continued to pump out In one sense it is no bad thing: it removes an mutant organism being able to destroy an 6 (”greening of downs were to come. To get as far as it has, life 6 the continents”) STINKING, SEWER- the continents”) n oxygen, there came a point where the balance embarrassing billion-plus year delay between entire planetary ecosystem – the first biogenic 4 on Earth was even luckier than we thought. 4 LIKE SEAS tipped inexorably towards oxygen, and the cyanobacteria arising and oxygen levels in the climate disaster,” says Kirschvink. 2 excess finally accumulated in the air. Perhaps it air first taking a significant upwards turn. In this And yet the great oxygenation was oxygen Atmospheric Nick Lane is the first Provost’s Venture Research Atmospheric oxygen oxygen Atmospheric 0 took the 300 million years leading up to the great level) today’s of (percentage 4 3 2 1 0 Fellow at University College London, and author “great oxygenation event” of around 2.4 billion impermanent. The same chromium record level) today’s of (percentage 4 3 2 1 0 BILLION YEARS 2.7 bya 2.4 bya oxygenation event to get to that tipping point. years ago, levels rose from around 1 per cent of that provides evidence for a first whiff of BILLION YEARS 2.7 bya 2.4 bya 750 to 650 Animals of Life Ascending: The ten great inventions of AGO (bya) Cyanobacteria today’s levels to perhaps 10 per cent. oxygen 300 million years before this event AGO (bya) Cyanobacteria Great oxygenation event million years ago evolution (Profile, 2009)

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