The notion that life originated in hydrothermal vents was, for a long time, a sleepy area of scientific inquiry because the vents first found, known as "black smokers," were way too hot and acidic. But in 1989, Michael Russell, a British geochemist who now heads the Planetary, Chemistry and Astrobiology Group at NASA's Jet Propulsion Lab at Caltech, proposed the idea that there were also alkaline hydrothermal springs. He began exploring serpentinization -- a geochemical process where seawater circulating through oceanic crust reacts with minerals found there to produce hydrogen, etc., and warm alkaline fluids. Russell suspected that, in effect, serpentinization set the stage for life to emerge in Hadean times when the oceans were still anoxic and highly acidic. He envisioned that a Hadean ocean was also home to a protected environment in the form of porous, precipitous mounds produced by serpentinization. These hollow castles or submarine alkaline vents -- with their complex micro-compartments and channels separated by film-like mineral membranes -- could have served as a "hatchery" of first life with the right energetics, Russell believed.
Interest in Russell's now 25-year-old alkaline-spring hypothesis began to peak in 2000 with the discovery of Lost City, an actual alkaline hydrothermal vent system on top of the Atlantis Massif in the Atlantic Ocean. So far the Lost City system is unique.
The formation resembles hot wax paraffin plunged into a tub of cold water, or mini-volcanoes. But Lost City's internal fluid temperature is 50 to 90 degrees C. instead of 400 degrees C., as in black smokers. Marine geologist Deborah Kelley, who led the first expedition to Lost City, once described its fluid as "similar to liquid drain-o."
If, in fact, Russell's ancient submarine hatchery of life once existed, what could have been the bioenergetics, since ultraviolet radiation was unlikely to be the necessary spark?
Data collected from Lost City plus lab simulations by Russell and his collaborators, Wolfgang Nitschke (French National Center for Scientific Research [CNRS], Marseille), Elbert Branscomb (University of Illinois, Urbana-Champaign) et al. has led them to think that the energetics central to the emergence of life in the Hadean hatchery would not only have been the catalysis provided by metals, but also a power "conversion" magic due to proton flow involving the vent system's mineral membranes being exposed to alkaline conditions on one side and acidic seawater on the other.
The idea is that this movement of protons then got "baked in" to the emerging life system. The system remembered how to move protons to create fuel, which in today's life is ATP (adenosine triphosphate) -- all cells burn it to keep us alive. Russell, Branscomb et al. have elaborated on these points in recent articles published in Philosophical Transactions of the Royal Society B and Astrobiology journal.
Indeed, says University College London biochemist Nick Lane, UV is the last thing life emerging at hydrothermal vents would have wanted. The thinking is that alkaline springs life would at first have been looking to stay close to home -- that is, in the hatchery, where the water was cool -- rather than venture out and about into an inhospitable world beyond the vent.
Lane recently co-authored a piece in Science on life's origin at hydrothermal vents with Bill Martin (University of Dusseldorf), who argues, contrary to Russell, Branscomb and Nitschke, that "metal ions alone" could have provided the necessary energetics to get life going.
Following are excerpts from my interviews on the origin of life at hydrothermal springs with Michael Russell and Elbert Branscomb, peppered with comments from Nick Lane. Bill Martin was on vacation at the time I spoke with Russell, Branscomb and Lane, and could not be reached for further comment. I'll be brief with introductions, since these are well-known personalities in science with lots to say.
Michael Russell pioneered the field of alkaline hydrothermal vents a quarter-century ago. He is a British geochemist with a Ph.D. from the University of Durham and has, for the last half-dozen years, been investigating alkaline springs theory at NASA's Jet Propulsion Lab at Caltech. Prior to that Russell was a research fellow at the Scottish Universities Environmental Research Center. He's also spent time prospecting for precious metals, among other great adventures, including studying volcanoes in the Solomon Islands.
Elbert Branscomb is a physicist at the University of Illinois, Urbana-Champaign, formerly chief scientist of the US DOE Genome Program, and before that a physicist at Lawrence Livermore National Laboratory. He was awarded the Edward Teller Fellowship in 2001 for his contribution to LLNL and DOE. Branscomb has a Ph.D. in theoretical physics from Syracuse University.
Nick Lane is a biochemist at University College London, where he investigates the origin of bioenergetics and the origin of life. He is also a masterful book author (Power, Sex, Suicide, and other provocative titles), winning the 2010 Royal Society Prize for Science Books, and symposium organizer, and he plays the Irish fiddle, among other talents. Nick Lane earned his Ph.D. from the University of London.
Suzan Mazur: Are we talking about the origin of life or the origin of bioenergetics?
Elbert Branscomb: One of the deep and controversial issues is in what sense are those the same question.
Suzan Mazur: You're saying the origin of life and the origin of bioenergetics are one and the same.
Elbert Branscomb: To an important degree, yes. Life is an incredible thousand-ring circus of twirlers and high-wire trapeze artists, a fury of non-equilibrium activity. It requires power to drive it. Our contention is it had to be that way right from the start, when the circus was vastly simpler, that the first step in life's origin was stumbling onto a solution to initiate power, overcoming an energetics challenge. The information side of life -- RNA, DNA, protein synthesis, polypeptides and the rest -- that came later; it's derivative.
The critical issues are: What were the exploitable sources of power the inanimate world supplied, and how were those sources of power tapped to drive the first high-wire chemical acts of the circus of life?
Several of the chemical activities needed for the most rudimentary metabolism, the most rudimentary biochemistries, are ones that cannot happen on their own. They have to be powered, driven against their thermodynamic will. Forced.
We think we have an idea where the power could have come from and how the hook-up happened.
Suzan Mazur: There are some substantial scientists with varied perspectives investigating the origin of life and bioenergetics at hydrothermal vents.
Elbert Branscomb: Yes. No important scientific question has ever been resolved by a conflict-free community walk in the park of objective "evidence." For example, there was that famous 30-year struggle in the field of bioenergetics known as the "ox-phos" wars over Peter Mitchell's idea of the proton motive force and the process he called chemiosmosis.
Proton motive force is a membrane-spanning difference in proton concentration -- a "gradient," or "disequilibrium" -- which living cells constantly drain and replenish using the power obtained by "burning" food.
It was Mitchell who realized that this gradient was used by life to drive the production of its main intracellular chemical fuel, ATP, which it uses in turn to power most of its intracellular circus. The proton gradient acts like water behind a dam. The disequilibrium is used to drive molecular generators as the protons flow downhill through a membrane. The generators are literally turbine-like rotary motors, molecular motors. They charge up the ATP chemical fuel system.
This was one of the most important discoveries made in the science of life, but battles over the idea persisted even after Mitchell got the Nobel Prize in 1978. Some of his opponents had to die for the fighting to come to an end.
Oddly, whereas Mitchell's idea was right on the principle, it was, in some basic respects, wrong on the mechanism. It was Paul Boyer who fundamentally got that part right, for which he was awarded the Nobel Prize in 1997.
Suzan Mazur: Michael, you trailblazed the serpentinization idea. Why do you think the earliest bioenergetics was proton gradients via serpentinization at alkaline hydrothermal vents rather than metal ions alone?
For example, Filipa Sousa, and Bill Martin -- a former collaborator of yours -- at the University of Dusseldorf, reported the following in a recent Elsevier paper:
First newer findings document eyebrow-raising similarities between the bioenergetics reactions of anaerobic autotrophs and geochemical reactions that occur spontaneously at some types of hydrothermal vents, an exciting development. Second, electron bifurcation has recently been discovered, a mechanism of energy conservation that explains how it is possible for acetogens and methanogens to reduce CO2 with electrons from H2, even though the first segment of the reaction sequence is energetically uphill.
Michael Russell: The reason why Elbert, Wolfgang and I think the proton motive force is important and have written recent articles -- one published by the Royal Society and the other a story for Astrobiology journal -- is because it's so peculiar that life would pump protons out of a cell just to have them return to generate an energy currency within the cell. It's rather like pumping water uphill just so you can use the free energy on the way downhill in a turbine to give you electricity. Why bother to pump them outside or up the gradient in the first place?
So we think it's because the conditions in which life started offered just this gradient for free. Life is stuck with this rather peculiar way of working. That is, microbial cells evidently have to pump protons out of the cell to get into the periplasm because those were the conditions at the very origin of life in one of these hydrothermal springs where the protons were already on the outside. So that was one point.
It's naïve for Sousa and Martin to say that these are new ideas. The idea is about 20 years old. We said this a long time ago. When they say "geochemical," what they're missing is: How do they get the methyl group, the CH3 group? All life has CH3, many CH3 groups amassed in its organic molecules. Our view is that it can't have been produced from the reduction of carbon dioxide, because the thermodynamic barrier is too high. And I notice now that they don't suggest that either, amazingly. But they suggest a geochemical origin after all. In their Biochimica et Biophysica Acta paper [cited above, published by Elsevier], they say that they are gaining their methyl group from hydrothermal means.
Suzan Mazur: The one I just quoted from where they say "it is possible for acetogens and methanogens to reduce CO2 with electrons from H2, even though the first segment of the reaction is energetically uphill."
Michael Russell: We agree with that, but the reduction only gets you carbon monoxide. It only takes away one oxygen from CO2. And I think they're saying the same thing. It only took one oxygen out of carbon dioxide to make carbon monoxide.
We suggested using electron bifurcation in 2009. Now suddenly Bill has adopted the idea, well-established in the literature, that electron bifurcation was significant, but I think we were first to say how significant it would be to the origin of life. We involved molybdenum as a redox bifurcating element in our 2009 paper. And then Bill wrote quite an extensive paper about electron bifurcation. So he kind of got into the same field as us.
What they're saying is they need a methyl group just like we do. If you look in the BBA paper, they will admit, in parentheses, that Tom McCollom says no methyl sulfides have been found in hydrothermal springs. And yet they say, well, there's methane there, so there must have been some methyl stuff.
Suzan Mazur: What about the point Bill Martin, Filipa Sousa and Nick Lane make in the recent Science magazine article "Energy at life's origin" about "the synthesis of high energy bonds that underpin substrate level phosphorylation can be catalyzed by metal ions alone--"
Michael Russell: I have no sympathy with that view at all. You can't "catalyze" the synthesis of "high energy bonds." Such syntheses have to be driven.
Suzan Mazur: "--and does not require either proteins or membranes whereas chemiosmotic synthesis of ATP requires both. This indicates that substrate phosphorylation came first in early bioenergetics evolution and powered the evolution of genes and proteins."
Michael Russell: There are just so many things laid out on the table here. Let me just address the one point about the methyl group. What they're saying is that they need methyl groups from geochemistry. That's their big thing. They've absolutely got to have it, and yet in the BBA paper in parentheses Tom McCollom says they've never been found. I presume Tom McCollom was a referee and that's why they had to put that in. I'm guessing that. So, in other words, they have no geochemical source for the methyl group, the CH3 group.
Nick Lane: I think we all agree that methyl sulfides could be important, whether they are delivered from the deep by serpentinization as CH3SH -- I don't know. Bill wants CH3SH out of the ground; there's not much evidence that it is available, but it would be surprising if it wasn't; Mike wants CH4 out of the ground, and we know that this does indeed emerge today from Lost City, but we can't be totally sure it is abiotic.
I want H2 out of the ground, some HS- and would like to react them all at the interface in the vent to form CH3SH and CO directly, driven by the proton gradient across thin semi-conducting inorganic barriers.
Suzan Mazur: Elbert has told me this:
The catalysis that Bill Martin is invoking is absolutely critical and a huge thing, but it couldn't provide the kind of coupling of outside sources of energy to the inside thermodynamic lift that I think is required.
Elbert Branscomb: What's wrong with resting the case on catalysis, the ability of metal ions, particularly in the precipitous mounds that are produced by the serpentinization mechanism -- the thing that is wrong in saying that's sufficient is that all that a catalyst can do is accelerate the rate of the reaction which would go on its own. To get life started, I think it is inarguable, and I think Lane would support that. Lane has argued that strongly himself many times that to get life started, you have to do more than just make chemistry go that would run on its own.
The wonderful thing about the Russell model is that it provides the proton gradient driver for free via geochemistry. Early life, therefore, did not have to do what we now all do, which is to get our mitochondria to recreate that proton gradient at great difficulty and expense to drive ATP.
Nick Lane: What Bill's specifically saying -- and the details do matter here, and that's why my name is on this [Science] piece -- is that chemiosmotic coupling with proteins across a membrane came later, across an organic membrane.
Suzan Mazur: When Bill Martin talks about "metal ions alone" and the earliest bioenergetics, what exactly is he referring to?
Nick Lane: He's referring specifically there to Huber and Wachterhauser's 1997 paper showing that, starting with carbon monoxide and methyl sulfides, you can produce things like acetyl phosphate, or at least methyl thioacetate, which is a thioester, and that was catalyzed by metal ions (Ni) and metal sulfides (FeS and NiS) alone. And so starting with the kind of carbon compounds that he wants the vent to be giving, which is to say carbon monoxide and methyl sulfides -- these activated methyl groups that he's talking about -- it's possible to drive everything from that. So that's what he means by that remark.
I would like to derive those methyl groups, methyl sulfide, etc., by the direct reduction of the interface in the vent. But from there on, I think it's the same chemistry that he's talking about, so the distinction there is quite small.
The distinction with what Mike is saying -- they are also deriving methane from the vents, but they're then using things like nitric oxide in the oceans to oxidize it to give a methyl group. So this is a distinct hypothesis which is assuming a much more oxidized early ocean than I would assume. But like I would do, it's assuming that it's being driven in the vent itself rather than coming from serpentinization.
Mike is looking to drive the formation of pyrophosphate within the walls themselves, whereas I would look to drive the formation of acetyl phosphate by the conditions that Bill is talking about but driven by the proton gradients.
They're all slightly different views of really rather a very small problem but a very difficult problem, because it's the source of all the organic carbon. It's the source of all the energy, all the carbon, and these are directly testable questions. And we're all trying to test it in different ways.
Suzan Mazur: So the difference between your work and what Mike Russell and Elbert Branscomb are doing -- there's not a huge divide.
Nick Lane: Not at all, Mike is the pioneer of this field. We differ on details, but the overall conception comes from Mike.
What Elbert Branscomb was saying in requiring a larger energetic push, and what Mike has always said, is that it requires not just a proton gradient but a redox gradient as well, and that the redox gradient is providing an extra "oomph" of power, which Bill and I do not have without the redox gradient. That's essentially what their argument is. He's saying we also need to have strong oxidizing agents -- nitric oxide or things like that -- in the ocean. And then you have both the redox gradients, you have hydrogen inside and nitric oxide outside -- there's a lot of energy in that couple, on the one hand. So you also have a proton gradient, pH 11 inside and pH 5 or 6 on the outside. There's a lot of energy in that as well.
My question about that is: The trouble is most of the organic chemistry that people talk about works very well in anoxic conditions. So getting hydrogen to react with CO2 and producing amino acids, etc. -- it's all favored under anoxic conditions. Now, I think they're playing a little bit fast and loose with what "anoxic" means. They're saying there's no oxygen there, but there is nitric oxide, which, in terms of its reduction potential, is very similar to oxygen. So they're claiming really microoxic conditions, in effect. Those themselves should inhibit the forward reaction to make organics. Now, they would say it will work if you have a compartmentalized system, and they may be right, but I think they're calling on something which is quite difficult to really imagine for me. So I would want to do without it, the reason being that to drive carbon reduction, for me, requires a continuous flux of protons across membranes or thin inorganic barriers; it is no use if the barrier retains an electrical potential over many hours. It needs to dissipate in seconds but be replenished in seconds too. If it's the case that protons flux that rapidly into the compartments, then nitric oxide would too. And if that's the case, then the compartments would be microoxic in their redox potential, so further carbon reduction to form amino acids, etc., would no longer be favored.
Suzan Mazur: Nigel Goldenfeld recently told me the following regarding life: "Once we understand why the thing can exist in the first place, then we can understand how it is instantiated in any particular system." Michael, are you saying you now understand why "the thing can exist" and "how it is instantiated" -- that it is somehow "baked in"? How do you envision life kicking in, how does the "I am in charge" moment happen?
Michael Russell: For my own private happiness, I think we have an idea of how life starts. I think it would start that way on any other planet because these wet, rocky worlds always have the same kind of ingredients, the same kind of disequilibria, the same kind of free energy gradients. So I'm quite happy about that. The only difference in the biochemistry would be at the cellular level, at the bacterial level, in what's called chirality -- that is, the handedness of the molecules, that they could be possibly a mirror image of the structures of our DNA and proteins. But overall life will always do the same job -- it hydrogenates carbon dioxide from the air or dissolved in water with hydrogen released either photochemically or geochemically from water to produce a small but ever-renewed amount of organic molecules. Only at the beginning would it require geochemical/hydrothermal methane.
Wittgenstein famously said, "Don't ask for meaning. Ask for use." Basically, life does a job for a world that's out of equilibrium. So, to me, it's kind of pretty straightforward, and I say we've got a good outline. I admit we don't have all the dots, but we feel we can trace it right through now from the geochemical environment, which is very far from equilibrium, right up to a bacterial cell. We recognize the stages, but of course there are big gaps in our knowledge and understanding.
I come from a geological point of view and think in terms of standing on a canyon side and looking across the canyon at established life as seen by the microbiologist. There are researchers on the other side, and I'm trying to "meet" them. We recognize huge similarities in terms of bioenergetics and the requirements for inorganic elements. We've got some stepping stones. They're rather far apart, but the stepping stones go right across the canyon. It's exactly opposite. As Schiller reportedly said, "and in the chasm lies the truth." Life employs so many things available at the submarine alkaline hydrothermal springs, such as metals and phosphorus, etc.
Suzan Mazur: You're talking about sparking life. You're going from something being "baked in," something being imposed on a system, and then that system comes alive; the system takes charge. How is that leap made? How does that happen?
Michael Russell: The kind of imagination I would bring to bear on this is that when you let out the bath water, within about six seconds billions upon billions of water molecules cooperate with each other going down the vortex, down the plug hole. That's called self-organization. The universe itself gets very quickly into ways of self-organizing when there are large gravity or electrical gradients or whatever. The universe organizes itself. To me life is not such a peculiarity; it's complex, but in a sense it is similar to the other mechanisms that get rid of or lower the energy gradients (increase the entropy) of the universe.
Suzan Mazur: So Nigel Goldenfeld's call for a general theory of life is what's needed, because we don't quite understand what life is.
Michael Russell: I would take the philosopher view that it's what things do that really matters. You don't know me very well, and I don't know you very well. But it's what we say that matters. We may never know each other that well. It's the same with all phenomena in the universe. We approach phenomena by use. We can see what they do. We can see the effect they have.
I look at it from that point of view, and then I try and understand the nitty-gritty of life and its origin once I have that sense of it.
Suzan Mazur: It's more relational than "I am in charge."
Michael Russell: Yes, it's relational. Absolutely.