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. Key Words: Origin of life-Prebiotic chemistry-Hydrothermal systems-Protocells-Progenotes-Microbial communities. Astrobiology 20, 429-452. ''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.''

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.

There is a general assumption that amphiphilic compounds, such as fatty acids, readily form membranous vesicles when dispersed in aqueous phases. However, from earlier studies, it is known that vesicle stability depends strongly on pH, temperature, chain length, ionic concentration and the presence or absence of divalent cations. To test how robust simple amphiphilic compounds are in terms of their ability to assemble into stable vesicles, we chose to study 10- and 12-carbon monocarboxylic acids and a mixture of the latter with its monoglyceride. These were dispersed in hydrothermal water samples drawn directly from hot springs in Yellowstone National Park at two pH ranges, and the results were compared with sea water under the same conditions. We found that the pure acids could form membranous vesicles in hydrothermal pool water, but that a mixture of dodecanoic acid and glycerol monododecanoate was less temperature-sensitive and assembled into relatively stable membranes at both acidic and alkaline pH ranges. Furthermore, the vesicles were able to encapsulate nucleic acids and pyranine, a fluorescent anionic dye. None of the amphiphiles that were tested formed stable vesicles in sea water because the high ionic concentrations disrupted membrane stability.

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