A (chemical) potential theory of life's origin

60 years ago, Stanley Miller, working with Harold Urey at the University of Chicago, US, published a paper that transformed our view of how life on Earth began.1 In their famous ‘prebiotic’ experiment, Miller and Urey subjected a mixture of hydrogen, water, methane and ammonia to electrical discharges, and found amino acids in the reaction products. Astronomer and author Carl Sagan called this ‘the single most significant step in convincing many scientists that life is likely to be abundant in the cosmos’.
As a model for how life could emerge from lifeless ingredients, the Miller–Urey experiment has not weathered so well. It is now generally accepted that their mixture does not reflect the likely composition of the Earth’s early atmosphere. And the scenario in which amino acids are cooked up in the sea by lightning has been rather eclipsed by a view that the fundamental components were brewed in the rich mix of compounds spewing forth from deep-sea hydrothermal vents, sheltered from the harsh environment at the planet’s surface. The arguments continue, but none detracts from the fact that Urey and Miller showed that producing complex prebiotic compounds was far from miraculous.

Starting blocks

Perhaps a more ambivalent legacy of that epochal experiment was that it inadvertently added to the tendency, launched contemporaneously by James Watson and Francis Crick, to view life in terms of chemical structure. Thus the focus of origin-of-life studies was placed on making life’s building blocks: amino and nucleic acids. This is of course (literally) a vital aspect, but it neglects the role of energetics in enabling life. For without a source of energy, prebiotic proteins and nucleic acids are just so much gunk.
‘Without a source of energy, proteins and nucleic acids are just so much gunk’
The pendulum is now swinging back, however, as exemplified by two recent meetings at the Royal Society on the bioenergetic aspects of life. Biochemist Nick Lane of University College London, UK, an organiser of both events, has recently collaborated with William Martin of the University of Düsseldorf, Germany, on a proposal for how the first organisms powered themselves.2
Lane and Martin favour the view that life arose at hydrothermal vents, not merely because these provide heat and the ingredients for making complex organics but because they create sustained gradients of ion concentration – of chemical potential – that can be harnessed to drive chemistry. 

Vive la difference

The organisms on the deepest branches of the phylogenetic tree of evolution are indeed chemiosmotic, deriving energy from differences in sodium and hydrogen ion (proton) concentrations across their membranes. A proton concentration gradient drives the formation of the biochemical ‘battery’ adenosine triphosphate (ATP) by the ATP synthase enzyme, which seems to have been a component of the last universal common ancestor of all life on Earth.3 In ‘primitive’ cells like this, the key metabolic process is the reduction of carbon dioxide to methane using electrons from hydrogen, coupled to the flow of protons through membrane-bound ATP synthase. 
But this enzyme is already a sophisticated piece of kit. How could that process have got going? Lane and Martin offer a detailed, plausible story.
The key is iron sulfide, a common mineral at hydrothermal vents. An iron–sulfur cluster is present in the protein ferrodoxin, which assists in that CO2 reduction reaction in some of the most ancient organisms. So iron sulfides inside the porous fabric of alkaline vents might have acted in a similar capacity before ferrodoxin. The process could have been driven by the ‘electrochemical battery’ created by a difference in proton concentration between the vent’s alkaline interior and the seawater outside, separated by a thin layer of the sulfide.
The researchers suggest that the molecules created this way might accumulate as membrane-like layers on the vent walls. But to escape the vent walls and exist as autonomous protocells, these membranes would have to relinquish their dependence on the vent’s ion gradients and sustain their own gradients using trans-membrane pumps. Lane and Martin suggest that the membranes could have developed a sodium pump called an antiporter, in which the movement of protons down the concentration gradient from seawater into the vent pumps sodium ions ‘uphill’ in the other direction. Such membrane proteins are common in cells today. The continuous efflux of alkaline fluid would ensure that the proton gradient persists. 
Ideas like this are necessarily speculative. The real value of this one is that it presents the emergence of life as an energetic rather than an informational problem. As the researchers put it very strikingly: ‘Life is not so much a reaction as a side reaction of the cell’s core bioenergetic process.’


1  S L Miller, Science, 1953, 117, 528 (DOI: 10.1126/science.117.3046.528)
2 N Lane and W F Martin, Cell, 2012, 151, 1406 (DOI: 10.1016/j.cell.2012.11.050)
3 A Y Mulkidjanian et al, Nat. Rev. Microbiol., 2007, 5, 892 (DOI: 10.1038/nrmicro1767)

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