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. 2012 Apr 3;109(14):E821-30.
doi: 10.1073/pnas.1117774109. Epub 2012 Feb 13.

Origin of first cells at terrestrial, anoxic geothermal fields

Armen Y Mulkidjanian  1 , Andrew Yu Bychkov, Daria V Dibrova, Michael Y Galperin, Eugene V Koonin
Affiliations

Origin of first cells at terrestrial, anoxic geothermal fields

Armen Y Mulkidjanian et al. Proc Natl Acad Sci U S A. .

Abstract

All cells contain much more potassium, phosphate, and transition metals than modern (or reconstructed primeval) oceans, lakes, or rivers. Cells maintain ion gradients by using sophisticated, energy-dependent membrane enzymes (membrane pumps) that are embedded in elaborate ion-tight membranes. The first cells could possess neither ion-tight membranes nor membrane pumps, so the concentrations of small inorganic molecules and ions within protocells and in their environment would equilibrate. Hence, the ion composition of modern cells might reflect the inorganic ion composition of the habitats of protocells. We attempted to reconstruct the "hatcheries" of the first cells by combining geochemical analysis with phylogenomic scrutiny of the inorganic ion requirements of universal components of modern cells. These ubiquitous, and by inference primordial, proteins and functional systems show affinity to and functional requirement for K(+), Zn(2+), Mn(2+), and phosphate. Thus, protocells must have evolved in habitats with a high K(+)/Na(+) ratio and relatively high concentrations of Zn, Mn, and phosphorous compounds. Geochemical reconstruction shows that the ionic composition conducive to the origin of cells could not have existed in marine settings but is compatible with emissions of vapor-dominated zones of inland geothermal systems. Under the anoxic, CO(2)-dominated primordial atmosphere, the chemistry of basins at geothermal fields would resemble the internal milieu of modern cells. The precellular stages of evolution might have transpired in shallow ponds of condensed and cooled geothermal vapor that were lined with porous silicate minerals mixed with metal sulfides and enriched in K(+), Zn(2+), and phosphorous compounds.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
A terrestrial geothermal system (scheme based on refs. 52, 53, 62, 138) that is fed mostly by water from rain and snow (meteoric water) which, when it is deep underground, mixes with cation- and anion-enriched magmatic fluids and becomes heated to 300 to 500 °C; such hot fluids can leach diverse ions from the hot rock. Upon heating, the water becomes lighter and, being enriched in metal cations and such anions as Cl−, HS−, and CO32−, ascends toward the surface. At shallower depths, the rising hot water starts to boil because of lower pressure. The vapor phase usually separates from the liquid phase, which leads to the typical zoning (53, 62). The separation is not only physical but also chemical; e.g., whereas Cl− anions mostly stay in the liquid phase, the gaseous compounds, such as CO2, NH3, and H2S, redistribute into vapor. The flow route of the liquid phase and the exact point of its discharge are determined by the crevices within the rock; the ejected fluids are characterized by slightly alkaline pH and high content of chloride and sodium, which both can be traced to the contribution of magmatic waters. The vapor rises upward and spreads within the rock; the subsurface area that is filled by steam and gas is called the vapor-dominated zone. Part of the steam condenses near the surface and is ejected by the thermal springs, and the rest of the steam reaches the surface through fissures of the rock to form fumaroles (i.e., steam vents). Metal cations are carried both by the liquid and by the vapor phases (52, 53), although the K+/Na+ ratio is higher in the vapor phase (Table 2).
Fig. 2.
Fig. 2.
Evolution of protocells at a primordial anoxic geothermal field. (A) Anoxic geothermal field over a terrestrial geothermal system; the figure corresponds to the boxed section in Fig. 1. A primordial geothermal system could form over a “hot spot,” similar to modern Island (139) or a primitive subduction zone (52, 69, 70, 140). The cooling of the ascending, H2S-enriched vapor causes precipitation of metal sulfides, particularly pyrite, which starts beyond the surface. At the point of water/vapor discharge, H2S starts to escape into the atmosphere, thus increasing the pH of the discharging fluids. By analogy with modern geothermal fields, the geothermal fluids and condensed vapor are expected to run down the slope, cool down and loose transition metals through sulfide precipitation. At neutral pH, Cu2S, PbS, and FeS2, shown by dark colors, should have precipitated first (–73), leaving Mn and Zn ions in the liquid phase. The relief depressions gave rise to lakes, ponds or puddles; at a certain distance from the thermal springs, after the cooling of geothermal fluids and the fall-out of Cu2S, PbS, and FeS2, these basins should have became particularly enriched in Zn2+ and Mn2+ ions, with their beds covered by ZnS and MnS-containing silicate minerals (shown by yellow color). (B) An anoxic geothermal pond as a sink for diverse (organic) substrates delivered by geothermal fluids and abiotically (photo)synthesized at minerals. These substrates could be consumed by protocells that are shown dwelling in the deeper, UV protected layers of the pond bed, within inorganic compartments build of silica minerals and metal sulfide particles.
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