Promotion of protocell self-assembly from mixed amphiphiles at the origin of life

Jordan, Sean; Rammu, Hanadi; Zheludev, I.N.; Hartley, Andrew M.; Maréchal, Amandine; Lane, Nick

doi:10.1038/s41559-019-1015-y

Cited by 131 publications

(143 citation statements)

References 72 publications

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“…In our current study we show that a temperature increase significantly accelerates the formation of membrane compartments and further initiates their fusion, which supports the recent findings of Jordan et al 7 . The accelerated nucleation and growth lead to maturation of compartments, which eventually establish physical contact.…”

supporting

confidence: 93%

“…This temperature range also represents the conditions in warm ponds: 50-80 °C 42 . Recent evidence shows that the mixtures of single chain amphiphiles form vesicles most readily at temperatures of ~70 °C in aqueous solutions containing mono-and divalent cations in broad pH range 7 . In the light of these observations, it appears that warm temperatures of ponds or LCHFs can allow and even favor protocell compartmentalization.…”

Section: Impact Of Temperature In the Context Of Origin Of Lifementioning

confidence: 99%

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Rapid growth and fusion of protocells in surface-adhered membrane networks

Köksal

Liese

Xue

et al. 2020

Preprint

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Elevated temperatures might have promoted the nucleation, growth and replication of protocells on the early Earth. Recent reports have shown evidence that moderately high temperatures not only permit protocell assembly at the origin of life, but could have actively supported it. Here we show the fast nucleation and growth of vesicular compartments from autonomously formed lipid networks on solid surfaces, induced by a moderate increase in temperature. Branches of the networks, initially consisting of self-assembled interconnected nanotubes, rapidly swell into microcompartments which can spontaneously encapsulate RNA fragments. The increase in temperature further causes fusion of adjacent networkconnected compartments, resulting in the redistribution of the RNA. The experimental observations and the mathematical model indicate that the presence of nanotubular interconnections between protocells facilitates the fusion process.The important role of solid surface support for the autonomous formation of primitive protocells has been suggested earlier in the context of the origin of life 1,2 . Hanczyc, Szostak et al. showed that vesicle formation from fatty acids was significantly enhanced in the presence of solid particle surfaces consisting of natural minerals or synthetic materials 1,2 . Particularly the silicate-based minerals accelerated the vesicle generation.In a recent report, we showed the autonomous formation and growth of surface adhered protocell populations as a result of a sequence of topological transformations on a solid substrate 3 . Briefly, upon contact with a mineral-like solid substrate, a lipid reservoir spreads as a double bilayer membrane. The distal membrane (upper -with respect to the surface-) ruptures and forms a carpet of lipid nanotubes. Over the course of a few hours, fragments of these nanotubes swell into giant, strictly unilamellar vesicular compartments. This relatively slow process is entirely self-driven and only requires a lipid reservoir as source, a solid surface, and surrounding aqueous media. The resulting structure consists of thousands of lipid compartments, which are physically connected to each other via a

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supporting

confidence: 93%

Section: Impact Of Temperature In the Context Of Origin Of Lifementioning

confidence: 99%

Rapid growth and fusion of protocells in surface-adhered membrane networks

Köksal

Liese

Xue

et al. 2020

Preprint

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“…Mineral cavities within vent rock formations have also been proposed to serve as compartments for primitive forms of life (Lane and Martin, 2012;Russell et al, 2014;Weiss et al, 2016). A recent report demonstrated that certain selected lipid mixtures could assemble into vesicles at 70C in the alkaline water of ''white smoker'' vents ( Jordan et al, 2019). Monnard and Deamer (2002) also showed that specialized lipid mixtures could form stable membranes in seawater at ordinary temperatures and pH ranges.…”

Section: Figmentioning

confidence: 99%

The Hot Spring Hypothesis for an Origin of Life

2020

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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.''

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“…The hydrothermal vent hypothesis which has been criticized for allowing excessively high temperatures, salinity and pH gradients is, after the discovery of "Lost City"-type hydrothermal fields (LCHFs), being reconsidered 42 . LCHFs accommodate temperatures between 40 and 90 °C, which could have promoted the formation of prebiotic membrane compartments 43 . In our study, temperature increase weakens membrane-surface adhesion and causes immediate surface de-wetting 17 , facilitating the subcompartment formation.…”

Section: Temperature-enhanced Formationmentioning

confidence: 99%

Subcompartmentalization and pseudo-division of model protocells

Spustová

Köksal

Ainla

et al. 2020

Preprint

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Membrane enclosed intracellular compartments have been exclusively associated with the eukaryotes, represented by the highly compartmentalized last eukaryotic common ancestor. Recent evidence showing the presence of membranous compartments with specific functions in archaea and bacteria makes it conceivable that the last universal common ancestor and its hypothetical precursor, the protocell, could have exhibited compartmentalization. To our knowledge, there are no experimental studies yet that have tested this hypothesis. We report on an autonomous subcompartmentalization mechanism for protocells which results in the transformation of initial subcompartments to daughter protocells. The process is solely determined by the fundamental materials properties and interfacial events, and do not require biological machinery or chemical energy supply. In the light of our findings, we propose that similar events could have taken place under early Earth conditions, leading to the development of compartmentalized cells and potentially, primitive division.The origin of the eukaryotic cell is closely associated with the development of subcompartments, which create specific micro-environments to spatially or temporally regulate biochemical reactions, simultaneously. Until recently, cellular compartmentalization was associated solely with eukaryotic systems. Recent evidence shows that membrane-enclosed compartments also exist in other domains of life, such as in Archaea and Bacteria 1,2 . Archaea, for example, have acidocalcisomes, the membrane enclosed electron-dense granular organelles rich in calcium and phosphate, which is crucial for osmoregulation and calcium homeostasis 3 . In Cyanobacteria, membrane-bound thylakoids 4 , have been identified as compartments in which the light-dependent reactions of photosynthesis take place.Despite the differences between eukaryotic and prokaryotic compartments in terms of structural and functional complexity, the presence of membranous compartments in Procaryota 1 establishes a possibility of compartments having existed in protocells, and being evolutionarily conserved. There is essentially no experimental material, however, on how compartments could have consistently emerged from membranes in a prebiotic environment lacking membrane-shaping and -stabilizing proteins.Membrane-less laboratory models of cytoplasmic suborganization have been developed inside synthetic cells, i.e. giant unilamellar vesicles 5 . These models require moderately elaborate chemical systems. A few examples of the utilized materials and mechanisms to induce compartment formation involve thermo-responsive hydrogels 6 , pH driven protein (human serum albumin) localization 7 or a poly(ethylene glycol)-dextran aqueous two-phase system 8 . One study which report on the membrane-based multi-vesiculation inside amphiphilic compartments, has employed protein-ligand couples to induce this behavior, i.e. biotin-avidin conjugates 9 . Membrane-enveloped subcompartment formation in biological systems is therefore considered t...

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Promotion of protocell self-assembly from mixed amphiphiles at the origin of life

Cited by 131 publications

References 72 publications

Rapid growth and fusion of protocells in surface-adhered membrane networks

Rapid growth and fusion of protocells in surface-adhered membrane networks

The Hot Spring Hypothesis for an Origin of Life

Subcompartmentalization and pseudo-division of model protocells

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