The breath of life and death Nature, 24th October 2002 Thomas B.L. Kirkwood

Thomas B.L. Kirkwood reviews Oxygen: The Molecule that Made the World by Nick Lane. Original at Nature

The brilliant French chemist Antoine Lavoisier is credited with being the first to demonstrate the importance of oxygen to the world, showing in a famous experiment that the Holy Roman Emperor’s diamonds were safe at high temperature provided that oxygen was excluded. Tragically, Lavoisier survived this flirtation with danger only to lose his head to the guillotine in revolutionary Paris on trumped-up charges of false accounting. Over the following centuries, oxygen named for its ‘acid-forming’ powers, has become an element widely cherished for its life-supporting properties. We tend to see oxygen in a positive light, with superstar Michael Jackson allegedly spending his nights in an oxygen tent. Few other elements can claim this level of celebrity endorsement, but the truth is that oxygen is a mixed blessing. Anyone whose life has been marred by fire knows how dangerous it can be, and although we would quickly die without it, growing evidence suggests that oxygen plays a leading part in the ageing process. It is this balance of good and bad that makes oxygen such an interesting molecule.

Nick Lane’s enjoyable and informative book would have us believe that “without the threat of oxygen toxicity, life would never have evolved beyond a green slime”. Although we depend on it now, it seems highly likely that life first arose in the absence of oxygen. Oxygen strips organic molecules of electrons and the earliest replicating biopolymers would have been defenceless against its attack. Thus, life began anaerobically and it was during the quiet aeons of early biological evolution that the first photosensitising bacteria began to secrete oxygen as a ‘toxic’ metabolic waste. Not for the last time, the planet’s dominant life form made a mess of the environment. This environmental stress imposed a strong selection pressure and there emerged organisms that not only could withstand oxygen toxicity but which found in this pollutant the source of a new energy supply. Oxidative phosphorylation was entrained in the service of a new breed of life, and, in time, we came along.

In the first half of the book, Lane reviews in some detail the evidence for this role of oxygen in the evolution of life. Although he endorses the major elements of the conventional tale, he prefers a plot line that is relatively new. Instead of a primordial atmosphere made up mainly of methane, ammonia and hydrogen, Lane subscribes to the idea that 4 billion years ago the Earth’s atmosphere consisted mostly of nitrogen, as today, with some carbon dioxide and water vapour, and traces of other gases including oxygen. The common view – and mine before reading this book – is that the impressive armoury of defences against oxygen toxicity in present-day organisms evolved to counter the growing danger as free oxygen accumulated in the atmosphere. The alternative, favoured by Lane, is that oxidative stress was known long before free oxygen became a hazard. A significant source of oxidative stress comes from the actions of ultraviolet radiation on water molecules. If life established an early presence in the radiation-exposed ocean surface, where water-splitting photosynthesis might most feasibly have evolved, cells must quickly have acquired potent antioxidant enzymes, such as catalase. So, by the time atmospheric oxygen became a threat, the antioxidant defences were already in place.

Ultraviolet-induced oxidative stress remains a potent source of free radicals today, attacking any cell exposed to sunlight. Such stress is thought, for example, to play a part in age-related macular degeneration, one of the most important causes of visual impairment in older people. This brings us to the second half of Lane’s book, which is about oxygen’s role in killing us. It is a pity that this substantial aspect of the book is not hinted at by the subtitle, because Oxygen presents an entertaining and cogent account of how of how oxidative stress fits in to our rapidly expanding knowledge about ageing. Lane also describes work on degenerative conditions such as dementia, and explains with admirable clarity how an imbalance in the antioxidant defence system of people with Down’s syndrome, who have an extra copy of the gene for superoxide dismutase, the enzyme which tackles the dangerous superoxide radical but makes harmful hydrogen peroxide in the process, contributes to an increased risk of Alzheimer-like symptoms.

The one shortcoming of the book, perhaps inevitable given its title, is that Lane pushes one molecular player into the limelight, to the exclusion of others, more than is right. The argument that oxygen is the molecule that made the world is hard to swallow, and oxidative stress is not the only agent that makes us age. Nevertheless, Lane presents a nicely crafted account of an important element’s place in our lives. His book deserves to be widely read, even if, in time, it must share space on the bookshelf with equivalent books on carbon, nitrogen, iron, and the rest.