Too Much Oxygen

 

Once upon a time, oxygen levels on Planet Earth hit 35%. This purportedly took place circa 300 billion years ago as the Carboniferous period was giving way to the Permian. At the same time carbon dioxide levels were falling. One explanation is that carbon burial (coal formation) was especially rapid, and thus there was less carbon to combine with atmospheric oxygen to form carbon dioxide. Today, humans are reversing the process by extracting the coal and combusting it for energy.

 

What was special 300 billion years ago to cause this? It so happens to coincide with the formation of the supercontinent Pangaea with its wet climate and vast flood plains that favor the formation of coal swamps. The rise of trees with woody lignin-containing stems meant slow breakdown to release carbon because decomposing bacteria have a particularly hard time digesting lignin. I’m reading all this in Nick Lane’s Oxygen, a fascinating treatise that connects oxygen to energy, life, death, sex, and aging. I first read Lane’s book almost two decades ago, but I’m re-reading it again to refresh myself on interesting oxygen factoids to use as a theme in my upcoming Quantum chemistry class – which culminates in the unusual chemical bonding situation of molecular oxygen.

 

But back to our story on oxygen levels. Can we measure them from so long ago? We can certainly measure the carbon content in rocks from that era. And it is high, even after accounting for erosion and metamorphic processes. We can also measure the contents of air trapped in microscopic bubbles of ancient amber. (In Jurassic Park, dinosaur DNA was extracted from insects trapped in amber.) As a third measure, the relative proportion of carbon-12 and carbon-13 isotopes in limestone tells us how enriched the atmosphere was with oxygen. The evolution of plants and their selectivity for carbon-12 corroborates the story. While all these measures are indirect, taken together they strengthen the hypothesis of such high oxygen levels in the past.

 

Chapter 5 of Lane’s book, from which I’ve taken this information, is titled “The Bolsover Dragonfly: Oxygen and the Rise of the Giants”. There were huge insects in the Carboniferous period! Dragonflies and mayflies had wingspans approaching 20 inches; there were meter-long millipedes, and scarily large spiders (though not quite the size of Aragog). Megafauna! Or perhaps I should say Mesofauna. Was this all because of elevated oxygen levels? More oxygen, more energy, faster growth? Speculations abound, but the one I found most interesting is that the large size lengthened the diffusion of oxygen through the organism so that by the time it reached the mitochondria, the concentrations were much lower. Otherwise, oxygen poisoning would result.

 

There was practically no free oxygen at the origin of life on Earth. We are descended from single-celled prokaryotic hydrogen-breathers. Living systems can’t get as much metabolic energy from hydrogen as they can from oxygen. Aerobes thrive energy-wise while anaerobes live on subsistence. Molecular oxygen is unique with its oddly weak double bond making it thermodynamically stable; yet it is oddly kinetically stable despite being a diradical (with two unpaired electrons). It’s much stranger than it looks at first glance, and I’m hoping to take my P-Chem students through that story this coming semester.

 

Oxygen might be good for life, at least we aerobes think so. But we’ve also evolved a bag of tricks not to be poisoned by it. That’s the topic of Chapter 10 in Lane’s book: “The Antioxidant Machine: A Hundred and One Ways of Living with Oxygen”. Oxygen loves to accept electrons. It does so one electron at a time, forming superoxide and then hydrogen peroxide (by also stealing protons). When oxygen steals an electron from another molecule, the latter now has an unpaired electron and becomes reactive (kinetically unstable). It then tries to steal an electron from some other neighbor, and so on, potentially resulting in a cascading chain reaction. Anti-oxidant molecules halt this process, often by donating an electron to stabilize the radical.

 

To counter the effect of peroxidation reactions that are ultimately due to too much oxygen, there are multiple antioxidant strategies. Heme proteins (similar to hemoglobin) detect oxygen levels, “binding to excess oxygen and releasing it only slowly, maintaining a constant and low concentration of oxygen in the immediate environment.” Mucus secretion is a very effective strategy. In bacteria, the negatively charged polymers in the mucus capture positive metal ions, and these react with the marauding radicals. Biochemistry utilizes sulfur-containing compounds to react directly with peroxides or indirectly by regenerating antioxidant molecules such as vitamin C. Recently my research has focused attention on the role of sulfur-compounds in proto-metabolism so I’m learning a lot about this area. Lane’s discussion of the enzyme superoxide dismutase is now much more fascinating, compared to two decades ago when I lacked appreciation in my first reading of his book.

 

One thing you might be wondering: If oxygen levels were so high, shouldn’t there have been massive forest fires? And wouldn’t these have consumed the oxygen thereby maintaining balance? Lane tackles this head-on by estimating what would be needed to maintain the balance – the unrealistic total vaporization of all the forests. It turns out that forest fires tend to promote the burial of carbon and coal formation. Also, the previous estimates that oxygen levels above 25% would cause conflagration were dependent on setting moistened paper on fire. Paper has little lignin, and furthermore real plants accumulate silica which acts as a fire retardant. Turns out that more shiny coal indicates it was formed at higher temperatures likely with more oxygen in the atmosphere. The coal from the Carboniferous is particularly shiny, further evidence of high oxygen levels.

 

Oxygen is an enigmatic molecule. We aerobes can’t live without it, but it’s killing us at the same time it’s fueling our way of life. Lane spotlights this tension in his engaging and very readable book, peppered with fascinating anecdotes. Did you know that silica was used in paints as a fire retardant during the Second World War? Or that the males of many ants and bees are haploid possibly for similar reasons as human sperm? And if not for skin pigments such as melanin, you’d change from red to a blue hue when you engaged in vigorous bodily exertion? Lane provides memorable and colorful analogies. My favorite is his description of the Fenton reaction: “Hydrogen peroxide is a gangland thug. Normally quiet, posing little danger to casual passers-by, it turns violent on meeting a rival gang member. Damage to proteins containing embedded iron can be as swift and specific…” More importantly, I was reminded of how biochemistry tunes itself to avoid redox catastrophe. Living with oxygen is a fine balance indeed.