Mike Russell of NASA's Jet Propulsion Laboratory thinks that life originated in iron sulfide deposits located at ocean vents at some distance from submarine volcanoes. The interior of such deposits can be honeycombed with holes measuring a few hundredths of a millimeter across. Russell says these cavities would have concentrated hydrothermal fluids, allowing the precursors of proteins and RNA to form, while preventing this pre-biotic soup from leaking away into the ocean. The iron sulfide compartments also could have provided three-dimensional molds for the first cell walls.

In this interview, Mike Russell expands on his theory of how life came to be, and explains why he thinks "life from space" scenarios are dead wrong.

Astrobiology Magazine (AM): Let's first discuss your ideas about the origin of life.

Mike Russell (MR): The philosopher, given a puzzle, often asks not what is it, but what does it do? So what does life do? Life promotes reactions between molecules that are out of equilibrium to produce more stable molecules. At the same time, it generates a system that continues that process.

To my mind, the way to think about life is by following the geologist's dictum, "the present is the key to the past." The primary producers, cyanobacteria and plants, photosynthesize by reacting hydrogen from water with carbon dioxide in the atmosphere. Water, H2O, is split and the oxygen is released as waste while the hydrogen itself is split into 4 electrons and 4 protons, and those react with, and reduce, carbon dioxide.

But there is a deeper biosphere which also lives off carbon dioxide and hydrogen. In this case the hydrogen is generated from water by geochemical reactions, oftentimes in convection cells. That's the way life works now, and I would say it must have always been thus.

The modern fuel that we're interested in is hydrogen because we're worried about global warming. Well, the first fuel of metabolism was hydrogen. Early life used hydrogen and reacted with an oxidized gas. At that time there was no free oxygen, O2, so life used carbon dioxide, CO2.

It starts with a core reaction. Any theory of the origin of life needs a geochemical core reaction, but there's a kinetic barrier so it takes place slowly. You can have hydrogen and oxygen in the same room, and they're stable because of the kinetic barrier. It's only if you strike the match that you have a reaction. So hydrogen and carbon dioxide wanted to react but they had to face steep kinetic barriers, and life was the match that let them react together.

Studies of the origin of life area are peculiar. In any other area of science, you must get the initial conditions right. But many people seem to ignore the initial conditions at the origin of life, perhaps because they think it's some kind of miracle.

When people say to me that life came from other planets, or pre-biotic molecules were delivered from outer space and rained down into the ocean to make a little slick on the surface which was eventually energized to life by photons, I think that's hopeless. There's no core reaction.

It's like finding a dead whale on the beach -- you can't bring back to life even one of its cells. It's got DNA, RNA, lipids, peptides, broken-down proteins, but it's dead. How could we think that an oil slick comprised of organic dust from space could do any better?

AM: So you disagree with current theories regarding the spread of life in the universe by the dispersion of organic materials in comets?

MR: I think the current theories are lazy. They say for life to originate we need some organic molecules, and there's some up there in space, so maybe that'll do. That's just an extraordinary conclusion. No other branch of science works like this.

The temperature in space is very close to zero -- it's 2.4 Kelvin. It is true that sparse carbon-bearing molecules occasionally react through a process known as tunneling, but that hardly constitutes a proto-metabolism.

AM: But they're pre-biotic molecules.

MR: They're not! That is a really bad term. They're not on the way to anywhere. They may as well be excrement. The term "pre-biotic" is misleading, and I would love to see it dropped.

AM: So you think life can't arise from organic molecules in deep space?

MR: The organic molecules that make up the carbonaceous chondrites in space are mostly gunge. It's a Beilsteinian nightmare out there. Life works with a few building blocks. Look at a steel and concrete building. If you raze it down and then try to build another building out of the pieces, it would be a hopeless job. You'd do better constructing a new building out of simple raw materials.

This is how life had to start. You don't start with thousands upon thousands of organic molecules and end up with the 8 or so amino acids the earliest life needed. It's got to be from the bottom up, just like anything else.

If you find organic molecules elsewhere, for instance on Titan, then you don't need life. The organics are in a stable state. It's a mess; it's tar. The point is that life is what it does. It reacts hydrogen with carbon dioxide. That's why it's going to be the same everywhere.

The universe doesn't have too many shapes to choose from. There are spheres, hemispheres and spirals. Bubbles are rather like the first cells. Look at Art Nouveau. You'll find bubble upon bubble in many Art Nouveau pictures. That's the way we think easily of this kind of system.

Look at the Surrealists. The Surrealists decided to start from scratch after the first World War, because of the failure of western culture to prevent devastating war in Europe. One of the great Surrealists was Yves Tanguy. He worked for the Merchant Navy and he came back to Paris on holiday. He was on a tram and he saw a picture by de Chirico in a shop window.

He jumped off the tram, and he decided he was going to be an artist too. So he left the Navy and went back to Brittany, and he bought a house with a studio on top. He painted everything white, and he papered over the windows with white. He painted a picture called "Dehors," which means "outside." He painted outside from inside. He painted bubble structures called biomorphs, and he painted it in an ocean floor. That was in 1927.

That kind of system is not very different to the way that I think life began. I've made my children a chemical garden by dropping particular hydrated crystals into what's called water glass, or sodium silicate solution. You get bubble after bubble, lovely little structures, beautiful spires made of an inorganic silica membrane. Of course there were no organic molecules on the early Earth, but we have a way of making structures that look just like life. Nature has many bubble structures, and I say life started like a bubble.

Life is stuck in its history, and it can't do anything beyond its history. That's the way we can see our way back in evolutionary terms to the historical origin. The iron sulfide that we think comprised the first membrane is still with us, contained in nearly all membranes in life. It's the little bit of rock that reminds us where we come from - the rocky roots to the emergence of life.

AM: So you think life began within iron sulfide deposits as a chemical reaction that created stability from instability.

MR: It's only instability that creates structure. Without instability and energy, there is no form. We love structures that are far from equilibrium. We love to watch thunder storms and volcanic eruptions; we love to look at galaxies. These structures are generating disorder in the universe by being ordered themselves. The very fact that you have an ordered structure like life means that it can make a lot of disorder.

Another way of thinking about life is that it generates waste. Anyone with children will know what that's like -- we only have to look in our bins. And that's the waste we can see. Humans gathered together in a room can generate a lot of heat. This is all part of entropy.

So life is like a chemical vortex, with carbon dioxide and hydrogen disappearing down this vortex to make, for example, acetic acid. Acetogens do that to reach a stable state through chemical reactions, but first they have to get over a few kinetic barriers.

You need catalysts and a bit of extra energy to get to acetic acid. After getting to acetate, if you can get over another barrier, you can get all the way to methane, as do the methanoarchaea. Carbon dioxide plus hydrogen to methane generates even more energy, although it's more difficult than going from carbon dioxide and hydrogen to acetate.

So you can go to methane, or you can stop half way at acetate. It seems to me very likely that the kind of chemical reactions that became biochemical reactions were gelled by the regulating RNA or DNA systems, the coding systems that we need for life.

It's like having two different river channels on a mountain. Once the channel starts, then there's no way back, it's going to go downhill. So one part of the mountain range goes down one way, a watershed to methane, and another side goes down to acetic acid. And I would suggest they started at a similar time.

AM: The two different channels -- one that has a chemical reaction that led to acetic acid, and the other that led to methane -- eventually they led to the development of bacteria and archaea?

MR: Yes, you get the two prokaryotic domains. Then of course they get together by endosymbiosis at some later time to make the eukaryotes, making the third domain of life. AM: If life started in these iron sulfide cells, why would they want to ever break free from that constant supply of energy and nutrients provided by the vents?

MR: To use a popular American term, they were barely fit for purpose. They could just work. Iron sulfide is not a great catalyst, and iron sulfide minerals are also easy to oxidize and break. But if we can add a peptide that can organize itself around one of these iron sulfide structures, it will prevent crystallization and dissolution.

At the same time the surface-to-volume is closer to the optimum achieved by enzymes; in other words, the catalytic aspect of the iron sulfides is improved. Then we need to concentrate these peptidic structures, because modern cells are crowded with organic molecules. Peptides could also stick together to make amyloid. As such they would make good membranous material that could take over the role of the membrane from the iron sulfide.

But at first, bubbles of iron sulfide formed around a warm alkaline spring. When life originated, these bubbles were generated at the same time as organic materials, in very small amounts. The bubble is made of iron sulfide and some iron nickel sulfide.

That is the catalyst which allows the carbon dioxide from the outside percolating into the bubble to react with the hydrogen, which is coming out from the inside. While catalysis takes place in this inorganic membrane made of iron and nickel sulfides, we also need some energetic help, such as pyrophosphate, occurring today as adenine triphosphate, or ATP.

We make at least half our body weight in ATP every day; it is all-important. Part of the way ATP is generated is through something called the proton motive force. The protons on the outside come in through the membrane and they generate pyrophosphate, which is an energy storage. That's a kind of phosphate match. You can then use pyrophosphate to join molecules like amino acids together to make peptides.

You have to have everything happening at once. It's not a linear system. I like to call it a heterarchical system -- everything is required, and the molecules need to be interacting all at once. There's carbon dioxide, the hydrogen, the protons on the outside, the presence of phosphate, the amount of nickel iron sulfide catalyst that's precipitated. And it's a fresh catalyst because it's precipitated at exactly the same time the whole system is operating.

AM: Can you set up a Miller/Urey-type experiment with those conditions?

MR: We are trying to recreate these submarine hydrothermal conditions at JPL, but it's extremely difficult. At the time of life's origin on Earth, the carbon dioxide in the atmosphere was about 10 bars, and this made the ocean carbonic, with the pH of Cocoa Cola.

You also need hydrogen, but hydrogen doesn't dissolve in water that's near the surface, so in the lab you need 100 atmospheres bearing on the water to get the hydrogen into solution. You don't want the carbon dioxide and hydrogen fluids invading each other too quickly. Also, the bubbles are rather flimsy affairs, and you need to keep protons on the outside and alkaline solutions on the inside.

Another difficulty is keeping DNA out of the system. This planet is hopelessly compromised by living organisms. The people who try to sterilize space vehicles know how difficult that is. In addition, there wasn't any oxygen on the early Earth, so we have the problem of oxygen invading the system. So it's extremely hard to model, but I think it is possible to do it, and I think the Jet Propulsion Laboratory is the right place for that because we have common interests and concerns.

One reason why NASA works on the question of the emergence of life is because we want to look for life on other planets. But how can we do that if we don't know how life started on this planet? Any wet rocky planet will have the same chemical imbalances. We need to understand how that happens before we can look carefully at how life might exist elsewhere.

We spend tens to hundreds of millions of dollars to go to other planets to look for life. I'm all for that, but we've never really spent money on the emergence of life as a problem. We need chemists and physicists and microbiologists and biochemists and chemical engineers and electrochemists working on this, and they all would have to respect and try to understand each other's discipline.

I don't want to be handing data across the disciplinary divide. That's why I say I'm not too keen on interdisciplinary research; I want transdisciplinary research. I think we now know enough about the possibilities for the emergence of life to have a real stab at various experiments that would show whether these kinds of theories are plausible.

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