We present a testable hypothesis related to an origin of life on land in which fluctuating volcanic hot spring pools play a central role. The hypothesis is based on experimental evidence that lipid-encapsulated polymers can be synthesized by cycles of hydration and dehydration to form protocells. Drawing on metaphors from the bootstrapping of a simple computer operating system, we show how protocells cycling through wet, dry, and moist phases will subject polymers to combinatorial selection and draw structural and catalytic functions out of initially random sequences, including structural stabilization, pore formation, and primitive metabolic activity. We propose that protocells aggregating into a hydrogel in the intermediate moist phase of wet-dry cycles represent a primitive progenote system. Progenote populations can undergo selection and distribution, construct niches in new environments, and enable a sharing network effect that can collectively evolve them into the first microbial communities. Laboratory and field experiments testing the first steps of the scenario are summarized. The scenario is then placed in a geological setting on the early Earth to suggest a plausible pathway from life's origin in chemically optimal freshwater hot spring pools to the emergence of microbial communities tolerant to more extreme conditions in dilute lakes and salty conditions in marine environments. A continuity is observed for biogenesis beginning with simple protocell aggregates, through the transitional form of the progenote, to robust microbial mats that leave the fossil imprints of stromatolites so representative in the rock record. A roadmap to future testing of the hypothesis is presented. We compare the oceanic vent with land-based pool scenarios for an origin of life and explore their implications for subsequent evolution to multicellular life such as plants. We conclude by utilizing the hypothesis to posit where life might also have emerged in habitats such as Mars or Saturn's icy moon Enceladus. "To postulate one fortuitously catalyzed reaction, perhaps catalyzed by a metal ion, might be reasonable, but to postulate a suite of them is to appeal to magic." -Leslie Orgel.

The Hot Spring Hypothesis for an Origin of Life.

Over the last 70 years, prebiotic chemists have been very successful in synthesizing the molecules of life, from amino acids to nucleotides. Yet there is strikingly little resemblance between much of this chemistry and the metabolic pathways of cells, in terms of substrates, catalysts, and synthetic pathways. In contrast, alkaline hydrothermal vents offer conditions similar to those harnessed by modern autotrophs, but there has been limited experimental evidence that such conditions could drive prebiotic chemistry. In the Hadean, in the absence of oxygen, alkaline vents are proposed to have acted as electrochemical flow reactors, in which alkaline fluids saturated in H2 mixed with relatively acidic ocean waters rich in CO2, through a labyrinth of interconnected micropores with thin inorganic walls containing catalytic Fe(Ni)S minerals. The difference in pH across these thin barriers produced natural proton gradients with equivalent magnitude and polarity to the proton-motive force required for carbon fixation in extant bacteria and archaea. How such gradients could have powered carbon reduction or energy flux before the advent of organic protocells with genes and proteins is unknown. Work over the last decade suggests several possible hypotheses that are currently being tested in laboratory experiments, field observations, and phylogenetic reconstructions of ancestral metabolism. We analyze the perplexing differences in carbon and energy metabolism in methanogenic archaea and acetogenic bacteria to propose a possible ancestral mechanism of CO2 reduction in alkaline hydrothermal vents. Based on this mechanism, we show that the evolution of active ion pumping could have driven the deep divergence of bacteria and archaea.

The Origin of Life in Alkaline Hydrothermal Vents

Hydrothermal fields on the prebiotic Earth are candidate environments for biogenesis. We propose a model in which molecular systems driven by cycles of hydration and dehydration in such sites undergo chemical evolution in dehydrated films on mineral surfaces followed by encapsulation and combinatorial selection in a hydrated bulk phase. The dehydrated phase can consist of concentrated eutectic mixtures or multilamellar liquid crystalline matrices. Both conditions organize and concentrate potential monomers and thereby promote polymerization reactions that are driven by reduced water activity in the dehydrated phase. In the case of multilamellar lipid matrices, polymers that have been synthesized are captured in lipid vesicles upon rehydration to produce a variety of molecular systems. Each vesicle represents a protocell, an “experiment” in a natural version of combinatorial chemistry. Two kinds of selective processes can then occur. The first is a physical process in which relatively stable molecular systems will be preferentially selected. The second is a chemical process in which rare combinations of encapsulated polymers form systems capable of capturing energy and nutrients to undergo growth by catalyzed polymerization. Given continued cycling over extended time spans, such combinatorial processes will give rise to molecular systems having the fundamental properties of life.

https://www.mdpi.com/2075-1729/5/1/872/pdf

Coupled Phases and Combinatorial Selection in Fluctuating Hydrothermal Pools: A Scenario to Guide Experimental Approaches to the Origin of Cellular Life

Chemical gardens in laboratory chemistries ranging from silicates to polyoxometalates, in applications ranging from corrosion products to the hydration of Portland cement, and in natural settings ranging from hydrothermal vents in the ocean depths to brinicles beneath sea ice. In many chemical-garden experiments, the structure forms as a solid seed of a soluble ionic compound dissolves in a solution containing another reactive ion. In general any alkali silicate solution can be used due to their high solubility at high pH. The cation should not precipitate with the counterion of the metal salt used as seed. A main property of seed chemical-garden experiments is that initially, when the fluid is not moving under buoyancy or osmosis, the delivery of the inner reactant is diffusion controlled. Another experimental technique that isolates one aspect of chemical-garden formation is to produce precipitation membranes between different aqueous solutions by introducing the two solutions on either side of an inert carrier matrix. Chemical gardens may be grown upon injection of solutions into a so-called Hele-Shaw cell, a quasi-two-dimensional reactor consisting in two parallel plates separated by a small gap.

From Chemical Gardens to Chemobrionics

Prebiotic chemistry aims to explain how the biochemistry of life as we know it came to be. Most efforts in this area have focused on provisioning compounds of importance to life by multistep synthetic routes that do not resemble biochemistry. However, gaining insight into why core metabolism uses the molecules, reactions, pathways, and overall organization that it does requires us to consider molecules not only as synthetic end goals. Equally important are the dynamic processes that build them up and break them down. This perspective has led many researchers to the hypothesis that the first stage of the origin of life began with the onset of a primitive nonenzymatic version of metabolism, initially catalyzed by naturally occurring minerals and metal ions. This view of life's origins has come to be known as "metabolism first". Continuity with modern metabolism would require a primitive version of metabolism to build and break down ketoacids, sugars, amino acids, and ribonucleotides in much the same way as the pathways that do it today. This review discusses metabolic pathways of relevance to the origin of life in a manner accessible to chemists, and summarizes experiments suggesting several pathways might have their roots in prebiotic chemistry. Finally, key remaining milestones for the protometabolic hypothesis are highlighted.

/pdf/nonenzymatic-metabolic-reactions-and-life-s-origins-449369e1qi.pdf

Nonenzymatic Metabolic Reactions and Life's Origins.

Chemiosmotic coupling is universal: practically all cells harness electrochemical proton gradients across membranes to drive ATP synthesis, powering biochemistry. Autotrophic cells, including phototrophs and chemolithotrophs, also use proton gradients to power carbon fixation directly. The universality of chemiosmotic coupling suggests that it arose very early in evolution, but its origins are obscure. Alkaline hydrothermal systems sustain natural proton gradients across the thin inorganic barriers of interconnected micropores within deep-sea vents. In Hadean oceans, these inorganic barriers should have contained catalytic Fe(Ni)S minerals similar in structure to cofactors in modern metabolic enzymes, suggesting a possible abiotic origin of chemiosmotic coupling. The continuous supply of H2 and CO2 from vent fluids and early oceans, respectively, offers further parallels with the biochemistry of ancient autotrophic cells, notably the acetyl CoA pathway in archaea and bacteria. However, the precise mechanisms by which natural proton gradients, H2, CO2 and metal sulphides could have driven organic synthesis are uncertain, and theoretical ideas lack empirical support. We have built a simple electrochemical reactor to simulate conditions in alkaline hydrothermal vents, allowing investigation of the possibility that abiotic vent chemistry could prefigure the origins of biochemistry. We discuss the construction and testing of the reactor, describing the precipitation of thin-walled, inorganic structures containing nickel-doped mackinawite, a catalytic Fe(Ni)S mineral, under prebiotic ocean conditions. These simulated vent structures appear to generate low yields of simple organics. Synthetic microporous matrices can concentrate organics by thermophoresis over several orders of magnitude under continuous open-flow vent conditions.

https://link.springer.com/content/pdf/10.1007%2Fs00239-014-9658-4.pdf

An Origin-of-Life Reactor to Simulate Alkaline Hydrothermal Vents

Arsenic contamination of drinking water affects more than 140 million people worldwide. While toxic to humans, inorganic forms of arsenic (arsenite and arsenate), can be used as energy sources for microbial respiration. AioX and its orthologues (ArxX and ArrX) represent the first members of a new sub-family of periplasmic-binding proteins that serve as the first component of a signal transduction system, that's role is to positively regulate expression of arsenic metabolism enzymes. As determined by X-ray crystallography for AioX, arsenite binding only requires subtle conformational changes in protein structure, providing insights into protein-ligand interactions. The binding pocket of all orthologues is conserved but this alone is not sufficient for oxyanion selectivity, with proteins selectively binding either arsenite or arsenate. Phylogenetic evidence, clearly demonstrates that the regulatory proteins evolved together early in prokaryotic evolution and had a separate origin from the metabolic enzymes whose expression they regulate.

/pdf/a-new-family-of-periplasmic-binding-proteins-that-sense-8grtq5e9r0.pdf

A new family of periplasmic-binding proteins that sense arsenic oxyanions.

https://hal-amu.archives-ouvertes.fr/hal-01585207/document

Electron transfer through arsenite oxidase: Insights into Rieske interaction with cytochrome c.

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An Origin-of-Life Reactor to Simulate Alkaline Hydrothermal Vents

A new family of periplasmic-binding proteins that sense arsenic oxyanions.

Electron transfer through arsenite oxidase: Insights into Rieske interaction with cytochrome c.