Hydrothermal vent systems, which can support life in the absence of photosynthesis, are today inhabited by animals that form symbioses with lithoautotrophic microorganisms from which they obtain chemical energy. These hydrothermal systems might resemble the earliest microbial ecosystems on the Earth. Here, Martin, Baross, Kelley and Russell review how understanding these complex systems might inform our understanding of the origins of life itself. Submarine hydrothermal vents are geochemically reactive habitats that harbour rich microbial communities. There are striking parallels between the chemistry of the H2–CO2 redox couple that is present in hydrothermal systems and the core energy metabolic reactions of some modern prokaryotic autotrophs. The biochemistry of these autotrophs might, in turn, harbour clues about the kinds of reactions that initiated the chemistry of life. Hydrothermal vents thus unite microbiology and geology to breathe new life into research into one of biology's most important questions — what is the origin of life?

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Hydrothermal vents and the origin of life

The serpentinite-hosted Lost City hydrothermal field is a remarkable submarine ecosystem in which geological, chemical, and biological processes are intimately interlinked. Reactions between seawater and upper mantle peridotite produce methane- and hydrogen-rich fluids, with temperatures ranging from <40° to 90°C at pH 9 to 11, and carbonate chimneys 30 to 60 meters tall. A low diversity of microorganisms related to methane-cycling Archaea thrive in the warm porous interiors of the edifices. Macrofaunal communities show a degree of species diversity at least as high as that of black smoker vent sites along the Mid-Atlantic Ridge, but they lack the high biomasses of chemosynthetic organisms that are typical of volcanically driven systems.

https://science.sciencemag.org/content/sci/307/5714/1428.full.pdf

A Serpentinite-Hosted Ecosystem: The Lost City Hydrothermal Field

Chemistry of submarine hydrothermal solutions at 21 °N, East Pacific Rise

All life is organized as cells. Physical compartmentation from the environment and self-organization of self-contained redox reactions are the most conserved attributes of living things, hence inorganic matter with such attributes would be life's most likely forebear. We propose that life evolved in structured iron monosulphide precipitates in a seepage site hydrothermal mound at a redox, pH and temperature gradient between sulphide-rich hydrothermal fluid and iron(II)-containing waters of the Hadean ocean floor. The naturally arising, three-dimensional compartmentation observed within fossilized seepage-site metal sulphide precipitates indicates that these inorganic compartments were the precursors of cell walls and membranes found in free-living prokaryotes. The known capability of FeS and NiS to catalyse the synthesis of the acetyl-methylsulphide from carbon monoxide and methylsulphide, constituents of hydrothermal fluid, indicates that pre-biotic syntheses occurred at the inner surfaces of these metal-sulphide-walled compartments, which furthermore restrained reacted products from diffusion into the ocean, providing sufficient concentrations of reactants to forge the transition from geochemistry to biochemistry. The chemistry of what is known as the RNA-world could have taken place within these naturally forming, catalyticwalled compartments to give rise to replicating systems. Sufficient concentrations of precursors to support replication would have been synthesized in situ geochemically and biogeochemically, with FeS (and NiS) centres playing the central catalytic role. The universal ancestor we infer was not a free-living cell, but rather was confined to the naturally chemiosmotic, FeS compartments within which the synthesis of its constituents occurred. The first free-living cells are suggested to have been eubacterial and archaebacterial chemoautotrophs that emerged more than 3.8 Gyr ago from their inorganic confines. We propose that the emergence of these prokaryotic lineages from inorganic confines occurred independently, facilitated by the independent origins of membrane-lipid biosynthesis: isoprenoid ether membranes in the archaebacterial and fatty acid ester membranes in the eubacterial lineage. The eukaryotes, all of which are ancestrally heterotrophs and possess eubacterial lipids, are suggested to have arisen ca. 2 Gyr ago through symbiosis involving an autotrophic archaebacterial host and a heterotrophic eubacterial symbiont, the common ancestor of mitochondria and hydrogenosomes. The attributes shared by all prokaryotes are viewed as inheritances from their confined universal ancestor. The attributes that distinguish eubacteria and archaebacteria, yet are uniform within the groups, are viewed as relics of their phase of differentiation after divergence from the non-free-living universal ancestor and before the origin of the free-living chemoautotrophic lifestyle. The attributes shared by eukaryotes with eubacteria and archaebacteria, respectively, are viewed as inheritances via symbiosis. The attributes unique to eukaryotes are viewed as inventions specific to their lineage. The origin of the eukaryotic endomembrane system and nuclear membrane are suggested to be the fortuitous result of the expression of genes for eubacterial membrane lipid synthesis by an archaebacterial genetic apparatus in a compartment that was not fully prepared to accommodate such compounds, resulting in vesicles of eubacterial lipids that accumulated in the cytosol around their site of synthesis. Under these premises, the most ancient divide in the living world is that between eubacteria and archaebacteria, yet the steepest evolutionary grade is that between prokaryotes and eukaryotes.

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On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells

The existence of a symbiotic association between vestimentiferan tube worms from deep-sea hydrothermal vents and chemoautotrophic sulfur-oxidizing prokaryotes, based on histological and enzymatic evidence, is suggested.

http://science.sciencemag.org/content/sci/213/4505/340.full.pdf

Prokaryotic Cells in the Hydrothermal Vent Tube Worm Riftia pachyptila Jones: Possible Chemoautotrophic Symbionts.

Hydrothermal vents jetting out water at 380° ± 30°C have been discovered on the axis of the East Pacific Rise. The hottest waters issue from mineralized chimneys and are blackened by sulfide precipitates. These hydrothermal springs are the sites of actively forming massive sulfide mineral deposits. Cooler springs are clear to milky and support exotic benthic communities of giant tube worms, clams, and crabs similar to those found at the Galapagos spreading center. Four prototype geophysical experiments were successfully conducted in and near the vent area: seismic refraction measurements with both source (thumper) and receivers on the sea floor, on-bottom gravity measurements, in situ magnetic gradiometer measurements from the submersible Alvin over a sea-floor magnetic reversal boundary, and an active electrical sounding experiment. These high-resolution determinations of crustal properties along the spreading center were made to gain knowledge of the source of new oceanic crust and marine magnetic anomalies, the nature of the axial magma chamber, and the depth of hydrothermal circulation.

https://science.sciencemag.org/content/sci/207/4438/1421.full.pdf

East Pacific Rise: Hot Springs and Geophysical Experiments

Asteroid regolith strength: Role of grain size and surface properties

We present the results of a series of laboratory low-speed impacts (< 4 m s−1) of centimeter-sized spherical projectiles into simulated dry and icy regolith samples. The target material was comprised of JSC-1 (Johnson Space Center) lunar simulant grains in the size range 100–250 μm, mixed with similar-sized water ice grains. Impacts were performed under vacuum, either at room temperature for JSC-1 samples or at cryogenic temperatures (<150 K) for icy mixtures. We measured the ejecta masses from a collection plate and impact crater dimensions from post-impact crater photographs. We find that both the ejecta masses and crater diameters followed trends predicted by established scaling laws, albeit with different fitting parameters, and we were able to fit a strength regime π scaling to our measured crater diameters. The water ice in our target material took two forms: grains mixed with the regolith grains and frost from air condensation coating regolith grains. In both cases, the presence of water ice in the sample led to lower ejected masses and smaller crater sizes. In addition, our measured crater sizes were several orders of magnitude larger than expected for impacts into solid rock or water ice. Using our measured scaling parameters, we applied our findings to a planetary context for the study of secondary craters on icy moons, as well as eroding collisions occurring in Saturn’s rings. We found that the deviation of our measurements from solid targets and from commonly used scaling parameters allowed us to reconcile our measurements with the models in both cases.

C. Cox

Papers

East Pacific Rise: Hot Springs and Geophysical Experiments

Asteroid regolith strength: Role of grain size and surface properties

Low-speed Impacts into Ice–Dust Granular Mixtures