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

Nature Ecology & Evolution volume 3, pages 1705–1714 (2019)Cite this article

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Abstract

Vesicles formed from single-chain amphiphiles (SCAs) such as fatty acids probably played an important role in the origin of life. A major criticism of the hypothesis that life arose in an early ocean hydrothermal environment is that hot temperatures, large pH gradients, high salinity and abundant divalent cations should preclude vesicle formation. However, these arguments are based on model vesicles using 1–3 SCAs, even though Fischer–Tropsch-type synthesis under hydrothermal conditions produces a wide array of fatty acids and 1-alkanols, including abundant C10–C15 compounds. Here, we show that mixtures of these C10–C15 SCAs form vesicles in aqueous solutions between pH ~6.5 and >12 at modern seawater concentrations of NaCl, Mg2+ and Ca2+. Adding C10 isoprenoids improves vesicle stability even further. Vesicles form most readily at temperatures of ~70 °C and require salinity and strongly alkaline conditions to self-assemble. Thus, alkaline hydrothermal conditions not only permit protocell formation at the origin of life but actively favour it.

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Fig. 1: Mixtures of amphiphiles increase the pH range of vesicle formation.
Fig. 2: Fatty acid/1-alkanol mixtures form vesicles from pH 7 to pH 12.
Fig. 3: Encapsulation of fluorescent dyes confirms stable vesicle formation.
Fig. 4: Mixtures of amphiphiles lower the concentration needed to form vesicles by ~30-fold.
Fig. 5: Fatty acid/1-alkanol mixtures form vesicles in the presence of salt and divalent cations.
Fig. 6: Salts can promote the formation of filaments composed of vesicles formed from mixed amphiphiles.
Fig. 7: Mixtures of amphiphiles support vesicle formation under oceanic alkaline hydrothermal conditions.

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Data availability

All data are available in the main text, Extended Data Figs. 1–10 and the Supplementary Information.

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Acknowledgements

We thank M. Turmaine for assistance with NS-TEM, and B. Battaglia, F. Werner and D. Braben for discussions. We are grateful to the BBSRC (H.R., LIDo Doctoral Training Programme) and bgc3 for funding. A.M.H. and A.M. are funded by the Medical Research Council UK (Career Development Award grant no. MR/M00936X/1 to A.M.).

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Authors and Affiliations

  1. Centre for Life’s Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK

    Sean F. Jordan, Hanadi Rammu, Ivan N. Zheludev & Nick Lane

  2. Institute of Structural and Molecular Biology, Birkbeck College, London, UK

    Andrew M. Hartley & Amandine Maréchal

  3. Institute of Structural and Molecular Biology, University College London, London, UK

    Amandine Maréchal

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  1. Sean F. Jordan
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Contributions

N.L. supervised the work. S.F.J., H.R., I.N.Z., A.M.H., A.M. and N.L. conceived and designed the experiments. S.F.J., H.R., I.N.Z. and A.M.H. performed the experiments. S.F.J., I.N.Z., A.M.H. and A.M. contributed materials and analysis tools. S.F.J. and N.L. analysed the data. S.F.J. and N.L. wrote the paper.

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Correspondence to Nick Lane.

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Extended data

Extended Data Fig. 1 Schematic representation of three different states of amphiphiles in aqueous solutions and their general relationship to pH.

Blue shading highlights hydrophilic areas whereas pink shading represents hydrophobic areas. Fully deprotonated amphiphiles will form micelles with a hydrophobic interior and hydrophilic exterior. Mixtures of protonated and deprotonated amphiphiles can self-organise into bilayer membranes forming vesicles with an aqueous interior. Fully protonated amphiphiles form hydrophobic droplets in aqueous solutions.

Extended Data Fig. 2 Optical density plot for 10:1 fatty acid/1-alkanol mixture.

Plot of normalised absorbance at 480 nm versus pH for 5 mM 10:1 C10-C15 fatty acid/1-alkanol mixture.

Extended Data Fig. 3 NS-TEM micrograph of vesicles from 0.1 mM 1:1 C10-C15 fatty acid/1-alkanol mixture.

NS-TEM micrograph of 0.1 mM 1:1 C10-C15 fatty acid/1-alkanol mixture vesicles at pH 7.17 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 4 NS-TEM micrograph of vesicles from 0.1 mM 1:1 C10-C15 fatty acid/1-alkanol mixture.

NS-TEM micrograph of 0.1 mM 1:1 C10-C15 fatty acid/1-alkanol mixture vesicles at pH 8.29 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 5 Critical bilayer concentration (CBC) plots for 1:1 and 5:1 fatty acid/1-alkanol mixtures.

Plot of absorbance at 480 nm versus concentration for 1:1 C10-C15 fatty acid/1-alkanol mixture (a) and 5:1 C10-C15 fatty acid/1-alkanol mixture (b).

Extended Data Fig. 6 NS-TEM micrograph of vesicles from 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture in NaCl.

NS-TEM micrograph of 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture vesicles in 600 mM NaCl at pH 12.19 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 7 NS-TEM micrograph of vesicles from 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture in MgCl2.

NS-TEM micrograph of 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture vesicles in 50 mM MgCl2 at pH 11.83 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 8 NS-TEM micrograph of vesicles from 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture in CaCl2.

NS-TEM micrograph of 5 mM 1:1 C10-C15 fatty acid/1-alkanol mixture vesicles in 10 mM CaCl2 at pH 12.18 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 9 NS-TEM micrograph of vesicles from 5 mM 1:1:1 C10-C15 fatty acid/1-alkanol/C10 isoprenoid mixture vesicles in mixture of salts.

NS-TEM micrograph of 5 mM 1:1:1 C10-C15 fatty acid/1-alkanol/C10 isoprenoid mixture vesicles in mixture of salts (600 mM NaCl, 50 mM MgCl2, 10 mM CaCl2) at pH 11.73 (some examples of vesicles indicated by black arrows).

Extended Data Fig. 10 Size exclusion chromatography (SEC) plot for 1:1:1 C10-C15 fatty acid/1-alkanol/C10 isoprenoid mixture vesicles in mixture of salts.

Plot of fluorescence intensity versus fraction number following size exclusion chromatography of 5 mM 1:1:1 C10-C15 fatty acid/1-alkanol/C10 isoprenoid mixture vesicles in mixture of salts (600 mM NaCl, 50 mM MgCl2, 10 mM CaCl2) at pH 12 prepared in the presence of 5 mM calcein. The initial peak represents the vesicle fraction and is followed by the free calcein dye.

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Supplementary methods, Tables 1 and 2 and Figs. 1–14.

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Jordan, S.F., Rammu, H., Zheludev, I.N. et al. Promotion of protocell self-assembly from mixed amphiphiles at the origin of life. Nat Ecol Evol 3, 1705–1714 (2019). https://doi.org/10.1038/s41559-019-1015-y

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