The Hot Spring Hypothesis for an Origin of Life

Abstract

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.

Keywords: Hydrothermal systems; Microbial communities; Origin of life; Prebiotic chemistry; Progenotes; Protocells.

FIG. 1.

Metaphor for how a computer program can be developed without a programmer.

FIG. 2.

An artist's conception of a geyser-driven Hadean volcanic hot spring system in which cycles of evaporation and rehydration can occur. Inset A shows a ring of dried solutes on the mineral surfaces at the edge of a fluctuating pool. Inset B shows a boiling pool associated with a hot spring site on Mount Mutnovsky in Kamchatka, Russia. (Art credit Ryan Norkus; Photo credit Tony Hoffman.)

FIG. 3.

A local scale depiction of a volcanic land mass interacting with freshwater and saltwater conditions (inset: pool in Bumpass Hell on Mount Lassen California). Credit: Bruce Damer and Ryan Norkus.

FIG. 4.

Natural drying and rewetting cycles in a small pool supporting three phases of membranous encapsulation: a hydrated phase (top), inset: protocells containing DNA budding out of a dried mixture of DNA and phospholipid, stained with acridine orange; a gel phase (center), inset: freeze-fracture image of a lipid hydrogel with ∼50% water by weight showing lipid vesicles fusing into lamellae; and a dehydrated phase (bottom), inset: freeze-fracture image of anhydrous lipid lamellae of phosphatidylcholine. Micrographs credit: Deamer. (Image adapted from Damer, .)

FIG. 5.

An integrated three-phase scenario showing how membranes and polymers can self-assemble and coevolve driven by fluctuating hydrothermal conditions on the prebiotic Earth.

FIG. 6.

A cartoon representation of the emergence of functions within cycling protocell populations. The top of the figure represents a simplified order of emergence of these functions, executed by a combination of polymers. Figure (A) is a model early protocell with S (stabilizing) factors and P (pore forming) polymers. At some point, polymers that can function as catalysts must emerge, and the two illustrated here are metabolic (M), capable of catalyzing growth, and (R) self-replication. Figure (B) depicts budding protocells capturing various combinations of these polymers, which affect their survivability. Figure (C) is an abstract representation of a protocell containing a more evolved system of growing polymers controlled by feedback networks (F). This system triggers a polymer mechanism D that can duplicate minimally viable sets of these polymers and deliver them by division into daughter cells. If these daughter cells contain fully functional polymer systems and are able to grow and divide again, they form the first lines of living cells.

FIG. 7.

Integrating a prebiotic Hadean geological landscape with the chemistry of life's origins in hydrothermal fields and its subsequent adaptive pathways into early microbial communities. Credit: Bruce Damer and Ryan Norkus. (Image adapted from an earlier version in Damer, .)

FIG. 8.

Product diffusion between neighboring protocells and a network of interactions set up within protocell aggregates forming in the moist gel phase of a wet-dry cycle.

FIG. 9.

Alternative scenarios for an origin of life and adaptive pathways from freshwater hydrothermal field pools or saltwater hydrothermal vents to eukaryotes and land plants.

FIG. 10.

Left: Depiction of Enceladus, a moon of Saturn visited by the Cassini mission, which discovered plumes emerging through cracks in the south polar ice possibly indicating oceanic hydrothermal activity. Right: silica nodules discovered at Columbia Hills on Mars by the Spirit rover consistent with an ancient hydrothermal environment (credits: NASA/JPL-Caltech).