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Was Oxygen Once the Limiting Nutrient for Complex Life?

Graham Shields—

Whether it is phosphorus for fertiliser, iron for steel or carbon for fuel, humans devour the chemical elements we need to sustain our way of life. Since the Great Industrial Acceleration of the 1950s, the world we live in has changed drastically; a tangible consequence of human consumption. In recent years we are becoming increasingly aware that we are using up finite resources day by day. If only resources were as plentiful as the air we breathe. . . .

Although we seldom regard it as such, oxygen is also a finite resource. Every year, we can measure how the carbon dioxide content of our atmosphere is rising due to the burning of fossil fuels and other human activities. Global warming and ocean acidification are the inevitable result. What is less well known, however, is that as carbon dioxide levels rise, oxygen levels fall. The carbon cycle seesaw tells us that our precious oxygen is a gift that can be taken away.

The first person to reveal the life-giving properties of oxygen was Joseph Priestley who suspected already in the latter half of the eighteenth century that air would turn out to be a mixture of different gases, and so set out to discover their individual properties. In a series of classic experiments in sealed bell jars, Priestley, an ordained minister from England, proved that plants give off a gaseous substance, without which mice cannot stay alive and candles cannot stay alight. In one fell swoop came the revelation that animals burn carbon, just like a fire burns coal. And both consume oxygen.

In the presence of sufficient oxygen, animals will thrive, but in its absence, they are either wholly absent or lie dormant, waiting for better times. It is for this reason that scientists frequently connect the evolution of our earliest air-breathing ancestors with the rise of an oxygenated atmosphere. There is, however, a fly in the bell jar.

Our earliest animal ancestors are now known to have appeared quite late in Earth’s long history. In fact, “we” took four billion years to emerge, but nobody quite knows why. There are two main reasons to doubt that a lack of oxygen caused this delay. Firstly, oxygen built up in earth’s atmosphere long before animals appeared in what is called the Great Oxidation Event, which occurred no later than 2.3 billion years ago; it would take another 1.7 billion years before anything resembling a worm first turned. Secondly, many simple animals, like mussels or sponges, can get by on very little oxygen. Although scepticism is healthy, I don’t think this tells the whole story.

On balance, I believe that insufficient oxygen was indeed an obstacle to animal evolution, but only in the magnitude of its flow through the surface environment, not its concentration. To show what I mean by that, let’s return to Joseph Priestley. In one of his famous experiments, he established that it was not the amount of oxygen, which curtailed aerobic metabolism, but the rate at which it was being produced. Priestley showed this by placing a lighted candle, sometimes with and sometimes without a plant, inside a sealed jar. He found that the candle did not burn for long, but with a plant inside, he could relight the wick 27 days after the candle had gone out. Although the plant’s presence caused oxygen to accumulate, it was not enough to keep the candle burning, no matter how much oxygen was there to start with.

This is a lot like Micawber’s principle, named after the likeable character in the Charles Dickens novel “David Copperfield”. Wilkins Micawber famously bemoaned his downtrodden circumstances, which came about due to his inability to live within his means. Nature is equally punishing, and like the money lenders, cannot abide an imbalance between earnings and outgoings. For a mouse to make its living inside a jar, there would need to be many plants to make sufficient oxygen. However, let’s not forget that plants also need resources, which we call nutrients. If these are in short supply, then not only would the plants’ growth be severely limited, but that of the animal, too.

Priestley clearly understood the ramifications of his discovery when he wrote in 1772 that “the injury which is continually done by such large number of animals is, in part at least, repaired by the vegetable creation”.1 In other words, without the continual production of oxygen by plants, through what we now call photosynthesis, not only humans, but the entire animal kingdom would perish.

To return to the origin of animals, it is therefore not enough to ask how much oxygen was around, or whether, if we had a time machine, a simple animal might be able to breathe. What is more important is whether such an aerobic metabolism, which continuously consumes precious oxygen, could be sustained. In other words, a world, in which animals can thrive, needs to be one in which plants are also able to grow sufficiently to sustain the flow of oxygen. But how do plants do this, when the Spring and Fall seem to balance the production and consumption of oxygen so perfectly?

The trick lies in the fact that not all plant life decays each fall. Some carbon is stored in wood, some of which may eventually even become coal, meaning that the oxygen once given by photosynthesis, is free to remain in earth’s oceans and atmosphere for hundreds, thousands or even millions of years. To resolve his sorry plight, Micawber needed desperately to up his productivity, just as a revitalised economy might haul a nation out of recession. By the same token, to evolve resource devourers like animals, plant productivity needed to change gear. The boost we needed was not just oxygen, but fertiliser.

There is no magic money tree for struggling economies, but just occasionally countries find a resource beneath their feet, be it oil or other mineral bounty, to boost their economies. Recent studies suggest that life got its own productivity surge during the Ediacaran Period of earth’s history around 600 million years ago in a time of extreme tectonic upheaval, when vast mountain belts scaled Himalayan heights. After more than a billion years of resource poverty, new volcanic chains belched out carbon dioxide, mountains rose and were eroded back down, shedding their nutrient loads into the sea. Life was plentiful because of the suddenly accelerated flow of resources.

Nutrient overload, or eutrophication, is what commonly happens today when nitrate and phosphate from fertiliser leaches out, sparking algal blooms that turn rivers, lakes and coastal areas anoxic. The same thing happened also in the Ediacaran Period when dead zones of extreme anoxia appeared beneath the fully oxygenated ocean surface. Indeed, the preservation of organic matter and mineral sulfide in such inhospitable places ensured that more oxygen was available to fuel the extraordinary radiation of animal life in other areas of the planet.

One valuable lesson of our shared backstory is that although vital resources are limited, life takes just about as much as it can. When a once limiting nutrient, like oxygen, suddenly becomes plentiful, fortune favours the opportunist who can make best use of the new resource. Animals won out when the flow of oxygen was no longer the most limiting factor to their success. However, mass extinctions later on in earth history remind us that mother earth is a fickle friend. What she gives with one hand, she can just as easily take away with the other.

Is oxygen the only secret behind animal evolution? No, the biggest mystery of all is how our earliest ancestors survived “Snowball Earth”, which was a time when our planet plunged into such a long, deep freeze that all life on earth was bound by thick ice for tens of millions of years. But that is a different story. . . . 

1. Joseph Priestley (1772) “Observations on different kinds of air.” Philosophical Transactions of the Royal Society, volume 62, pages 147-264.

Graham Shields is professor of geology at University College London. He lives in London, UK.

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