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. 2014 Apr;14(4):308-43.
doi: 10.1089/ast.2013.1110. Epub 2014 Apr 3.

The Drive to Life on Wet and Icy Worlds

Free PMC article

The Drive to Life on Wet and Icy Worlds

Michael J Russell et al. Astrobiology. .
Free PMC article


This paper presents a reformulation of the submarine alkaline hydrothermal theory for the emergence of life in response to recent experimental findings. The theory views life, like other self-organizing systems in the Universe, as an inevitable outcome of particular disequilibria. In this case, the disequilibria were two: (1) in redox potential, between hydrogen plus methane with the circuit-completing electron acceptors such as nitrite, nitrate, ferric iron, and carbon dioxide, and (2) in pH gradient between an acidulous external ocean and an alkaline hydrothermal fluid. Both CO2 and CH4 were equally the ultimate sources of organic carbon, and the metal sulfides and oxyhydroxides acted as protoenzymatic catalysts. The realization, now 50 years old, that membrane-spanning gradients, rather than organic intermediates, play a vital role in life's operations calls into question the idea of "prebiotic chemistry." It informs our own suggestion that experimentation should look to the kind of nanoengines that must have been the precursors to molecular motors-such as pyrophosphate synthetase and the like driven by these gradients-that make life work. It is these putative free energy or disequilibria converters, presumably constructed from minerals comprising the earliest inorganic membranes, that, as obstacles to vectorial ionic flows, present themselves as the candidates for future experiments. Key Words: Methanotrophy-Origin of life. Astrobiology 14, 308-343. The fixation of inorganic carbon into organic material (autotrophy) is a prerequisite for life and sets the starting point of biological evolution. (Fuchs, 2011 ) Further significant progress with the tightly membrane-bound H(+)-PPase family should lead to an increased insight into basic requirements for the biological transport of protons through membranes and its coupling to phosphorylation. (Baltscheffsky et al., 1999 ).


<b>FIG. 1.</b>
FIG. 1.
Diagrams showing the remelting of a thick volcanic plateau by a reinvigorated mantle plume, illustrating a delamination tectonomagmatic engine producing fresh ancient ocean crust on Earth continuously for 200–300 million years (Bédard, 2006). Left-hand cartoon shows molten magma (M1) generating a thick volcanic crust. This same batch of magma also ponds at the base of the crust, where it differentially melts the more siliceous and less dense component of the preceding volcanic host to produce quartz-rich tonalitic melt (T1). The more magnesium-rich residue partially metamorphoses to dense eclogite which begins to sink (E1). The right-hand cartoon shows how the buoyant siliceous melt invades the plateau to produce acidic (silica- and nickel-rich) volcanism and accompanying hot springs that have the potential to dispense carbon dioxide to the atmosphere and metal-rich solutions to the ocean, respectively (and see Sobolev et al., 2005). At the same time the dense eclogite (E1) delaminates and falls into the mantle. The larger bodies bore channels that may be exploited by further rising hot mantle diapirs. Smaller delaminated bodies mix into the shallow upper mantle and catalyze the formation of a second mantle melt (M2). Extraterrestrial wet and icy worlds with interiors hot enough to produce mantle plumes and thereby new ocean crust as well as oxidized volatiles could also set the stage for the onset of metabolism and life (and see Gaidos, ; Pasek and Greenberg, 2012). Reproduced from Bédard (2006) with permission.
<b>FIG. 2.</b>
FIG. 2.
The candidate pH and redox disequilibria driving the onset of biochemistry on wet rocky worlds. Oxidized and acidic volatiles are supplied to the atmosphere and hydrosphere by volcanoes (top); acidic ∼400°C springs supply the metals and H2S to the ocean (lower left); iron and manganese from these springs are photooxidized (center); reduced entities exploited by emergent metabolism are mainly supplied in alkaline hydrothermal solution to a submarine precipitate mound (lower right) (Nealson and Saffarini, ; Douville et al., ; Proskurowski et al., ; Martin et al., ; Zahnle et al., 2007). These are the initial far-from-equilibrium conditions considered to have driven the onset of life.
<b>FIG. 3.</b>
FIG. 3.
Picture of the Hadean water world. The first ocean was ≥5 km deep, entirely submerging any proto-continents (Bounama et al., ; Elkins-Tanton, 2008). Inset sketch shows how a proto-biotic methanotrophic community could have been nurtured by the methane and hydrogen emanating at a submarine alkaline vent on the Hadean Earth's ocean floor. The polarity of the water world is similar to that of a prokaryote, generally reduced on the inside and oxidized on the outside so that electrons are transported by various mechanisms toward the exteriors of both (Russell and Hall, 1997). Protons (or acidic volatiles) are also continuously pumped to the exterior of both, the one through volcanoes and certain very hot springs, the other by various enzymes such as Complexes I, III, and IV. (Photographs courtesy of Minik Rosing and Billy Brazelton.)
<b>FIG. 4.</b>
FIG. 4.
Structural comparisons between transition element sulfides and oxides of the kind found in the precipitate membranes with the active sites of metalloenzymes present in the LUCA: (a) ferrous hydroxide [Fe(OH)2]n (cf. brucite)—prone to oxidation to ∼Fe2(OH)5 (fougèrite)—with methane monooxygenase, (b) greigite and acetyl coenzyme-A synthase, (c) violarite and CO dehydrogenase, (d) nickelian mackinawite and [Ni-Fe] hydrogenase (Mielke et al., ; Nitschke et al., 2013).
<b>FIG. 5.</b>
FIG. 5.
This electro-geochemical hydrothermal system occupying a growing compartmentalized mound evolves through mineral recognition and propagation processes leading, through an amyloidal takeover, to a cofactor world which transforms through the stringing of bases along a peptide-like backbone into the RNA world capable of Darwinian evolution and the emergence of fully fledged autotrophic life (Russell et al., ; Milner-White and Russell, ; Yarus, ; Goodwin et al., 2012).
<b>FIG. 6.</b>
FIG. 6.
(a) Schema to illustrate how the outer margins of a growing Hadean submarine hydrothermal alkaline mound could house carbon fixation engines. Electrons driving these engines are borne first by mass transfer in alkaline hydrothermal solution from the reduced crust as H2 and CH4 to the precipitate mound. Here they are split from H2 and CH4 at nickel sites in sulfides comprising the precipitate membranes and conducted via those sulfides and oxyhydroxides to interface high potential electron acceptors, especially nitrite and nitrate, while others reduce the low potential acceptor carbon dioxide aided by the proton gradient. (Just as convection requires a cold sink, emergent metabolism needs high potential electron sinks to operate.) The availability of these high potential acceptors nitrate and nitrite (dispersed cathodes)—although supplied continually through carburation and tidal currents—probably limits the rate of proto-metabolism (Nitschke and Russell, , ; Branscomb and Russell, 2013). (b) Diagram illustrating the similarities between the metabolic operations of Lost City Methanosarcinales (LCMS), as in the cell on the right, with the putative hatchery of life illustrated in Fig. 6a (Kelley et al., 2005). Acetate is also a possible waste product—a product consumed by another type of the same microbe, presumably in conditions of contrasting disequilibria (Hoehler and Alperin, ; Lang et al., ; Brazelton et al., 2011).
<b>FIG. 7.</b>
FIG. 7.
The engines that put metabolism on the road. Highly idealized deconstruction of Fig. 6a to reveal the hypothetical proto-bioelectronic and proto-bioprotonic circuitry and channels in the inorganic membrane that feed the redox and proton disequilibria to the putative carbon-fixing and pyrophosphatase nanoengines (cf. Szent-Györgyi, , ; Poinsignon, ; Nitschke and Russell, 2013). Nickel sites in the FeS comprising the innermost zone of the inorganic membrane oxidize the hydrothermal H2, sending waves of electrons through the semiconducting iron minerals toward the oxidants bathing the membrane exterior. The resulting protons react with the hydroxyls in the hydrothermal fluid to produce more water. Some of the electrons reduce nitrate and nitrite to highly active NO and N2O at a molybdenum site stabilized by protons [e.g., [Fe2S2(MoS4)2]4- and/or [FeO(OH)(MoS4)2]3- (Itaya et al., ; Helz et al., 2013)], which in turn are hypothesized to oxidize methane to methanol on green rust [fougèrite, Fe2(OH)5, cf. Martinez-Espinosa et al., ; Starokon et al., 2011]. Two more electrons reduce MoVI atoms to MoIV, which then bifurcate; one electron is drawn along a large entropy-increasing path to FeIII in fougèrite comprising the membrane exterior, while the other takes the entropy-decreasing path against membrane potential and reduces the low potential nickel iron sulfide (e.g., Fe5NiS8). These reduced NiFe4 clusters then feed electrons to CO2 and formaldehyde in preparation for the assembly of CO and a methyl group to activated acetate, the entry point to putative carbon-fixing denitrifying methanotrophic acetogenesis. Fougèrite may also act as a proton pyrophosphatase. Note that while the characteristics of the alkaline ∼10 mM hydrothermal feed of electron donors remain stable for ≥1017 μs (i.e., ≥32,000 years, Ludwig et al., 2011), the concentrations of the oxidants are likely to vary widely in time and be the limiting entities in completing the circuit. The ocean may also have supplied many mM of SiO2 and a few mM of H2S to the alkaline hydrothermal chimneys (Mielke et al., ; Shibuya et al., 2010). Based on Nitschke and Russell (2013) and Russell, Nitschke and Branscomb (2013).
<b>FIG. 8.</b>
FIG. 8.
Calculated Gibbs energies of reaction for total cellular constituents assumed to be generated on mixing of Hadean seawater with a Lost City–like hydrothermal fluid as a function of temperature (Amend and McCollom, 2009). Fatty acid synthesis is exergonic at all temperatures, whereas amino acid synthesis is exergonic above ∼27°C, and strongly so between 30°C and ∼90°C. Amines and saccharides are potential products close to equilibrium. The synthesis of nucleotides, in strong contrast, is endergonic at all temperatures for all mixtures (Amend and McCollom, , Tables I, IV, and V). This is why life does not live on RNA/DNA alone, could not have begun relying on these molecules in these conditions, and why these polymers could never clog up the cell. Redrawn from Fig. 2 in Amend and McCollom (2009), with permission.

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