Life: An accident waiting to happen

The first and best-understood step in biogenesis — science’s answer to the other Genesis — was the rampant production of life’s molecular building blocks: sugars, amino acids, lipids and more. These raw materials formed as lightning pierced the atmosphere, as volcanic heat boiled in the deep ocean and ultraviolet radiation bathed molecular clouds in deep space. The seas of ancient Earth became increasingly concentrated in the stuff of life as biomolecules rained from the skies and rose from the depths.

The modern era of origins-of-life research began in 1953 with what remains to this day as the most famous experiment in biogenesis. The University of Chicago chemistry professor Harold Urey and his resolute graduate student Stanley Miller designed an elegant tabletop glass apparatus. Gently boiling water proxied for the hot Hadean ocean, a mixture of simple gases formed a primitive atmosphere, while electric sparks mimicked lightning. After a few days, the confined, colorless water turned pinkish, then brown with a complex mix of organic molecules. The transparent glass became smeared with sticky black organic sludge rich in amino acids and other bio-building blocks. Here was the fabled primordial soup, on a desk top. Miller’s 1953 paper announcing the results generated headlines around the world. Chemists soon flocked to the study of prebiotic chemistry.

Miller’s influence was strong. He and his followers dominated the origins-of-life community for more than three decades, until the late 1980s and the discovery of deep-sea “black smoker” ecosystems, far from the sunlit surface. Here, mineral-rich fluids interact with the hot volcanic crust to create ocean-floor geysers. Jets of scalding water contact the frigid deep ocean to create a constant rain of microscopic minerals (the particles that produce the “black smoke”). Life abounds in these astounding hidden places, fuelled by chemical energy at the interface between crust and ocean.

Step one in life’s origins turns out to be easy; every ancient environment with sources of energy and small carbon-bearing molecules probably produced its share of amino acids, sugars, lipids and other key ingredients. An atmosphere laced with lightning or exposed to harsh radiation works. So do black smokers and other deep, hot environments. Biomolecules form during asteroid impacts, from exposure to cosmic rays, and on sun-drenched dust particles high in the atmosphere. They even emerge in the frigid, deep-space molecular clouds that preceded the formation of our Solar System — places where microscopic dust particles are bathed in ultraviolet radiation. Tons of that organic-rich dust still rain down on Earth’s surface every year, as they have for more than 4.5 billion years. Life’s building blocks litter the cosmos.

The second stage of life’s origins involved selecting, concentrating, and assembling the ubiquitous bio-bits from the dilute prebiotic soup into life’s macromolecules — structures that can enclose a living cell and promote its chemical reactions. Two complementary processes probably played a role: self-assembly and template-directed synthesis.

Some distinctively elongated molecules with a skinny backbone of carbon atoms clump together spontaneously. These molecules include lipids, which can self-assemble into membranes encapsulating tiny cell-sized spheres, not unlike microscopic oil drops in water. In one of the most influential origins publications in history, the Californian biochemist David Deamer extracted a suite of these versatile organic molecules from the carbon-rich Murchison meteorite, which hit southern Australia in 1969. Deamer found that these molecules rapidly organised themselves into cell-like spheres. A few years ago, he and I found a similar result for carbon-rich molecules formed under black smoker conditions. Most origins scientists now agree that lipid self-assembly must have played a key role in life’s origins.

Most other bio-building blocks don’t self organise, but they concentrate on the safe, protective surfaces of rocks and minerals. Our experiments reveal that life’s molecular building blocks stick onto virtually any natural mineral surface, including all of Earth’s most common rock-forming minerals. And when several molecules compete for the same surface, they often cooperate to produce complex surface structures that may promote even more adsorption and more organisation. Details of prebiotic self-organisation are still a frontier of origins research, but self-assembly must have occurred on the primitive Earth in virtually every wet, chemically diverse environment.

Macromolecules were everywhere, but they were not alive until they could make copies of themselves. The greatest enigma in the biogenesis story remains the emergence of the first self-replicating system of molecules. Life’s most distinctive hallmark is reproduction: one consortium of molecules becomes two, two become four, and on and on in geometric expansion. Experiments have replicated portions of plausible reproductive cycles, though we have yet to mimic completely that elusive biochemical trick in the lab. The emergence of the first self-replicating system of molecules remains the greatest enigma in the biogenesis story. Nevertheless, at some point in space and time an organised collection of molecules began to duplicate itself at the expense of other molecules (ie “food”).

Why would a collection of molecules spontaneously start copying itself? The answer lies in the twin evolutionary pillars of variation and selection. Systems evolve because they display vast numbers of different possible configurations — that’s variation; and some of those configurations are much more likely to survive than others — that’s selection. Prebiotic processes produced hundreds of thousands of different molecules, but not all molecules were created equal. Some were relatively unstable and were quickly eliminated from the competition. Others clumped together in useless tar-like masses and floated away or sank to the ocean floor. But some molecules proved especially stable, even more so when they could bind to others of their kind or to a particularly tempting mineral surface. These molecules survived, as the prebiotic soup moved gradually from pure chemistry towards biology.

Scientists use three competing models to describe the first self-replicating system of molecules. The simplest (and therefore the one many of us prefer) is based on the ubiquitous citric acid cycle. Start with acetic acid with two carbon atoms plus CO2 to form pyruvic acid with three carbon atoms, which in turn reacts with CO2 to make the four-carbon oxaloacetic acid. Other reactions produce progressively larger molecules up to citric acid with six carbon atoms. The cycle becomes self-replicating when citric acid spontaneously splits into two smaller molecules, acetic acid plus oxaloacetic acid, which are also part of the molecular loop. One cycle of molecules thus becomes two, two become four, and so on. What’s more, many of life’s essential molecules, including amino acids and sugars, are readily synthesised by simple reactions with the core molecules of the cycle. Just add ammonia to pyruvic acid, for example, and you get the essential amino acid alanine. Every living cell on Earth incorporates the citric acid cycle, so it may well be a primordial characteristic — a chemical fossil descended from the very first life form.

At the opposite extreme of chemical complexity is the self-replicating autocatalytic network, a model championed by Stuart Kauffman at the Santa Fe Institute. The prebiotic soup initially incorporated hundreds of thousands of different small carbon-based molecules from varied sources. Some of those chemicals catalysed reactions that made new molecules, while other reactions accelerated the breakdown of their neighbours. An autocatalytic network consists of a collection of thousands of molecules that speed up the production of themselves, while destroying any molecule not in the network. It’s the molecular equivalent of “the rich get richer”. The network effectively makes copies of itself.

A third scenario, favored by the majority of biologically trained origins researchers, is the RNA world — a model based on a hypothetical strand of the genetic molecule RNA that makes copies of itself. RNA can simultaneously fulfil life’s two most critical functions: metabolism (making stuff) and genetics (transferring information on how to make stuff from one generation to the next). Of all life’s varied molecules, RNA is the one that does it all. The RNA world model rests on the assumption that some as yet poorly understood chemical mechanism produced vast numbers of different strands of RNA, and one of these myriad strands learned how to make copies of itself.

It probably took millions of years for that first crudely self-replicating molecular system to emerge, whether a citric acid cycle, an autocatalytic network, or self-replicating RNA. But unimaginable numbers of molecular combinations were being tried on trillions of trillions of mineral surfaces, across almost 200 million square miles of the Earth’s surface, for many millions of years. Some place, some time, one of those inconceivably immense numbers of molecular combinations worked. It learned to self-replicate and evolve. It became alive.

Self-replicating molecules insured their own survival by producing more-or-less identical daughters. What’s more, the molecular copying process was inevitably messy, so some of those copies were mutants. And while most mutations were lethal or conferred no significant advantage, a few fortuitous individuals outshone their parent, and thus the system evolved. Simply by copying errors, the original self-replicating molecule must have produced offspring that tolerated more extreme conditions of pressure or heat or salt, or replicated faster, or found new sources of food, or destroyed their less fit neighbours. The first self-replicating molecules engulfed Earth’s nutrient-rich zones in a geological instant.

By our planet’s one-billionth birthday, life had established a firm foothold on Earth’s surface, and it was poised to transform our planetary home.

Robert M. Hazen is senior staff scientist at the Carnegie Institution’s Geophysical Laboratory in Washington DC. This article is adapted from his recent book, The Story of Earth: The First 4.5 Billion Years, from Stardust to Living Planet (Viking, £17.50)