Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Heated gas bubbles enrich, crystallize, dry, phosphorylate and encapsulate prebiotic molecules

Abstract

Non-equilibrium conditions must have been crucial for the assembly of the first informational polymers of early life, by supporting their formation and continuous enrichment in a long-lasting environment. Here, we explore how gas bubbles in water subjected to a thermal gradient, a likely scenario within crustal mafic rocks on the early Earth, drive a complex, continuous enrichment of prebiotic molecules. RNA precursors, monomers, active ribozymes, oligonucleotides and lipids are shown to (1) cycle between dry and wet states, enabling the central step of RNA phosphorylation, (2) accumulate at the gas–water interface to drastically increase ribozymatic activity, (3) condense into hydrogels, (4) form pure crystals and (5) encapsulate into protecting vesicle aggregates that subsequently undergo fission. These effects occur within less than 30 min. The findings unite, in one location, the physical conditions that were crucial for the chemical emergence of biopolymers. They suggest that heated microbubbles could have hosted the first cycles of molecular evolution.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: DNA accumulation at gas bubbles in a thermal gradient.
Fig. 2: DNA accumulation by capillary flow.
Fig. 3: Ribozyme catalysis triggered by an interface.
Fig. 4: Sequence-selective gelation of RNA and DNA.
Fig. 5: DNA and RNA encapsulation and protection in vesicles formed at the interface.
Fig. 6: Crystallization and bubble movement.
Fig. 7: Dry–wet cycles and phosphorylation of nucleosides.

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available within the paper and its Supplementary Information. Additional information and files are available from the corresponding author upon reasonable request. X-ray crystallographic data were also deposited at the Cambridge Crystallographic Data Centre (CCDC) under CCDC deposition no. 1847429.

Code availability

The complete details of both simulations are documented in the html report and mph simulation files in the Supplementary Information.

References

  1. Schrödinger, E. What is Life? The Physical Aspect of the Living Cell (Cambridge Univ. Press, 1944).

  2. Cross, M. C. & Hohenburg, P. Pattern-formation outside of equilibrium. Rev. Mod. Phys. 65, 851–1112 (1993).

    Article  CAS  Google Scholar 

  3. Bodenschatz, E., Pesch, W. & Ahlers, G. Recent developments in Rayleigh–Benard convection. Annu. Rev. Fluid Mech. 32, 709–778 (2000).

    Article  Google Scholar 

  4. Fritts, D. C. & Alexander, M. J. Gravity wave dynamics and effects in the middle atmosphere. Rev. Geophys. 41, 1003 (2003).

    Article  Google Scholar 

  5. Eaton, J. K. & Fessler, J. R. Preferential concentration of particles by turbulence. Int. J. Multiph. Flow 20, 169–209 (1994).

    Article  CAS  Google Scholar 

  6. Götzendorfer, A., Kruelle, C. A., Rehberg, I. & Svenšek, D. Localized subharmonic waves in a circularly vibrated granular bed. Phys. Rev. Lett. 97, 198001 (2006).

    Article  Google Scholar 

  7. Chen, J. & Lopez, J. A. Interactions of platelets with subendothelium and endothelium. Microcirculation 12, 235–246 (2005).

    Article  CAS  Google Scholar 

  8. Moore, W. B. & Webb, A. A. G. Heat-pipe Earth. Nature 501, 501–505 (2013).

    Article  CAS  Google Scholar 

  9. Arndt, N. T. & Nisbet, E. G. Processes on the young Earth and the habitats of early life. Annu. Rev. Earth Planet. Sci. 40, 521–549 (2012).

    Article  CAS  Google Scholar 

  10. Duhr, S. & Braun, D. Why molecules move along a temperature gradient. Proc. Natl Acad. Sci. USA 103, 19678–19682 (2006).

    Article  CAS  Google Scholar 

  11. Baaske, P. et al. Extreme accumulation of nucleotides in simulated hydrothermal pore systems. Proc. Natl Acad. Sci. USA 104, 9346–9351 (2007).

    Article  CAS  Google Scholar 

  12. Niether, D., Afanasenkau, D., Dhont, J. K. G. & Wiegand, S. Accumulation of formamide in hydrothermal pores to form prebiotic nucleobases. Proc. Natl Acad. Sci. USA 113, 4272–4277 (2016).

    Article  CAS  Google Scholar 

  13. Kreysing, M., Keil, L., Lanzmich, S. & Braun, D. Heat flux across an open pore enables the continuous replication and selection of oligonucleotides towards increasing length. Nat. Chem. 7, 203–208 (2015).

    Article  CAS  Google Scholar 

  14. Mast, C. B., Schink, S., Gerland, U. & Braun, D. Escalation of polymerization in a thermal gradient. Proc. Natl Acad. Sci. USA 110, 8030–8035 (2013).

    Article  CAS  Google Scholar 

  15. Morasch, M., Braun, D. & Mast, C. B. Heat-flow-driven oligonucleotide gelation separates single-base differences. Angew. Chem. Int. Ed. 55, 6676–6679 (2016).

    Article  CAS  Google Scholar 

  16. Keil, L. M. R., Möller, F. M., Kieß, M., Kudella, P. W. & Mast, C. B. Proton gradients and pH oscillations emerge from heat flow at the microscale. Nat. Commun. 8, 1897 (2017).

    Article  Google Scholar 

  17. Budin, I., Bruckner, R. J. & Szostak, J. W. Formation of protocell-like vesicles in a thermal diffusion column. J. Am. Chem. Soc. 131, 9628–9629 (2009).

    Article  CAS  Google Scholar 

  18. Lerman, L. Potential role of bubbles and droplets in primordial and planetary chemistry. Orig. Life Evol. Biosph. 16, 201–202 (1986).

    Article  Google Scholar 

  19. Ariga, K. & Hill, J. P. Monolayers at air–water interfaces: from origins-of-life to nanotechnology. Chem. Rec. 11, 199–211 (2011).

    Article  CAS  Google Scholar 

  20. Eickbush, T. H. & Moudrianakis, E. N. A mechanism for the entrapment of DNA at an air–water interface. Biophys. J. 18, 275–288 (1977).

    Article  CAS  Google Scholar 

  21. Griffith, E. C. & Vaida, V. In situ observation of peptide bond formation at the water–air interface. Proc. Natl Acad. Sci. USA 109, 15697–15701 (2012).

    Article  CAS  Google Scholar 

  22. Deegan, R. D. et al. Capillary flow as the cause of ring stains from dried liquid drops. Nature 389, 827–829 (1997).

    Article  CAS  Google Scholar 

  23. Smith, K. A. On convective instability induced by surface-tension gradients. J. Fluid Mech. 24, 401–414 (1966).

    Article  Google Scholar 

  24. Batchelor, G. K. An Introduction to Fluid Dynamics (Cambridge Univ. Press, 1973).

  25. Deegan, R. D. Pattern formation in drying drops. Phys. Rev. E 61, 475–485 (2000).

    Article  CAS  Google Scholar 

  26. Larson, R. G. Transport and deposition patterns in drying sessile droplets. AIChE J. 60, 1538–1571 (2014).

    Article  CAS  Google Scholar 

  27. Savino, R., Paterna, D. & Favaloro, N. Buoyancy and marangoni effects in an evaporating drop. J. Thermophys. Heat Transf. 16, 562–574 (2002).

    Article  CAS  Google Scholar 

  28. Drobot, B. et al. Compartmentalised RNA catalysis in membrane-free coacervate protocells. Nat. Commun. 9, 3643 (2018).

    Article  Google Scholar 

  29. Weinberg, M. S. & Rossi, J. J. Comparative single-turnover kinetic analyses of trans-cleaving hammerhead ribozymes with naturally derived non-conserved sequence motifs. FEBS Lett. 579, 1619–1624 (2005).

    Article  CAS  Google Scholar 

  30. Dahm, S. C. & Uhlenbeck, O. C. Role of divalent metal ions in the hammerhead RNA cleavage reaction. Biochemistry 30, 9464–9469 (1991).

    Article  CAS  Google Scholar 

  31. Zhu, T. F. & Szostak, J. W. Coupled growth and division of model protocell membranes. J. Am. Chem. Soc. 131, 5705–5713 (2009).

    Article  CAS  Google Scholar 

  32. Budin, I. & Szostak, J. W. Physical effects underlying the transition from primitive to modern cell membranes. Proc. Natl Acad. Sci. USA 108, 5249–5254 (2011).

    Article  CAS  Google Scholar 

  33. Filonov, G. S., Moon, J. D., Svensen, N. & Jaffrey, S. R. Broccoli: rapid selection of an RNA mimic of green fluorescent protein by fluorescence-based selection and directed evolution. J. Am. Chem. Soc. 136, 16299–16308 (2014).

    Article  CAS  Google Scholar 

  34. Islam, S., Bučar, D.-K. & Powner, M. W. Prebiotic selection and assembly of proteinogenic amino acids and natural nucleotides from complex mixtures. Nat. Chem. 9, 584–589 (2017).

    Article  CAS  Google Scholar 

  35. Anastasi, C., Crowe, M., Powner, M. W. & Sutherland, J. D. Direct assembly of nucleoside precursors from two- and three-carbon units. Angew. Chem. Int. Ed. 45, 6176–6179 (2006).

    Article  CAS  Google Scholar 

  36. Jones, S. F., Evans, G. M. & Galvin, K. P. Bubble nucleation from gas cavities—a review. Adv. Colloid Interface Sci. 80, 27–50 (1999).

    Article  CAS  Google Scholar 

  37. Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).

    Article  CAS  Google Scholar 

  38. Lohrmann, R. & Orgel, L. E. Urea–inorganic phosphate mixtures as prebiotic phosphorylating agents. Science 171, 490–494 (1971).

    Article  CAS  Google Scholar 

  39. Gibard, C., Bhowmik, S., Karki, M., Kim, E.-K. & Krishnamurthy, R. Phosphorylation, oligomerization and self-assembly in water under potential prebiotic conditions. Nat. Chem. 10, 2012–2017 (2017).

    Google Scholar 

  40. Chow, Y. T. F., Maitland, G. C. & Trusler, J. P. M. Interfacial tensions of the (CO2+N2+H2O) system at temperatures of (298 to 448) K and pressures up to 40 MPa. J. Chem. Thermodyn. 93, 392–403 (2016).

    Article  CAS  Google Scholar 

  41. Sosson, M. & Richter, C. Enzyme-free genetic copying of DNA and RNA sequences. Beilstein J. Org. Chem. 14, 603–617 (2018).

    Article  CAS  Google Scholar 

  42. Forsythe, J. G. et al. Ester-mediated amide bond formation driven by wet–dry cycles: a possible path to polypeptides on the prebiotic earth. Angew. Chem. Int. Ed. 54, 9871–9875 (2015).

    Article  CAS  Google Scholar 

  43. Morasch, M., Mast, C. B., Langer, J. K., Schilcher, P. & Braun, D. Dry polymerization of 3′,5′-cyclic GMP to long strands of RNA. ChemBioChem 15, 879–883 (2014).

    Article  CAS  Google Scholar 

  44. Vaidya, N. et al. Spontaneous network formation among cooperative RNA replicators. Nature 491, 72–77 (2012).

    Article  CAS  Google Scholar 

  45. Mutschler, H., Wochner, A. & Holliger, P. Freeze–thaw cycles as drivers of complex ribozyme assembly. Nat. Chem. 7, 502–508 (2015).

    Article  CAS  Google Scholar 

  46. Soukup, G. A. & Breaker, R. R. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5, 1308–1325 (1999).

    Article  CAS  Google Scholar 

  47. Toppozini, L., Dies, H., Deamer, D. W. & Rheinstädter, M. C. Adenosine monophosphate forms ordered arrays in multilamellar lipid matrices: insights into assembly of nucleic acid for primitive life. PLoS One 8, e62810 (2013).

    Article  CAS  Google Scholar 

  48. Rajmani, S. et al. Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig. Life Evol. Biosph. 38, 57–74 (2008).

    Article  Google Scholar 

  49. Reineck, P., Wienken, C. J. & Braun, D. Thermophoresis of single stranded DNA. Electrophoresis 31, 279–286 (2010).

    Article  CAS  Google Scholar 

  50. Vargaftik, N. B., Volkov, B. N. & Voljak, L. D. International tables of the surface tension of water. J. Phys. Chem. Ref. Data 12, 817–820 (1983).

    Article  CAS  Google Scholar 

  51. Lide, D. R. CRC Handbook of Chemistry and Physics (CRC Press, 2001).

  52. Li, Y. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 33, 703–714 (1974).

    Google Scholar 

  53. Fell, C. J. D. & Hutchison, H. P. Diffusion coefficients for sodium and potassium chlorides in water at elevated temperatures. J. Chem. Eng. Data 16, 427–429 (1971).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank L. Keil for help with data analysis. Financial support from the Simons Foundation (318881 to M.W.P. and 327125 to D.B.), the German Research Foundation (DFG) through CRC/SFB 235 Project P07 and SFB 1032 Project A04, DFG Grant BR2152/3-1 and the US–German Fulbright Program is acknowledged. H.M. is supported by the MaxSynBio consortium, which is jointly funded by the Federal Ministry of Education and Research of Germany and the Max Planck Society. H.M. and K.L.V. are supported by the Volkswagen Initiative ‘Life?—A Fresh Scientific Approach to the Basic Principles of Life’. A.K. is supported by a DFG fellowship through the Graduate School of Quantitative Biosciences Munich.

Author information

Authors and Affiliations

Authors

Contributions

M.M., J.L., C.F.D., A.K., A.I. and Ph.S. performed the experiments. M.M., J.L., K.L.V., S.I., B.S., D.B.D., H.M., Pe.S., M.W.P., C.B.M. and D.B. conceived and designed the experiments. M.M., J.L., K.L.V., S.I., M.K.C., H.M., M.W.P. and D.B. analysed the data. M.M., J.L. and D.B. wrote the paper. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Dieter Braun.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

The Supplementary Information file contains additional experimental methods as well as all supplementary figures and tables and a brief description of all supplementary videos.

Supplementary Movie M1

Supplementary Video 1 shows the accumulation of a 132mer ssDNA strand in a 20 °C temperature difference at the contact line over time. In addition, the motion of 200 nm FAM-labelled polysterene beads tracking the flow profile of the chamber is shown.

Supplementary Movie M2

Supplementary Video 2 shows the accumulation of the Hammerhead ribozyme at the interface.

Supplementary Movie M3

Supplementary Video 3 shows the formation of a DNA hydrogel at the gas–water interface by self-complementary DNA. Also shown is the simultaneous accumulation of self-complementary RNA and non-complementary RNA.

Supplementary Movie M4

In Supplementary Video 4, 100 nm oleic acid vesicles were accumulated together with a 72mer DNA at the interface.

Supplementary Movie M5

Supplementary Video 5 shows a small bubble in a 150 µm-thick chamber filled with RAO.

Supplementary Movie M6

Supplementary Video 6 shows the accumulation inside a bubble at a temperature gradient of 20 °C.

Bubble Accumulation Simulation

The Simulation File contains both the upright (Cartesian) as well as horizontally aligned (cylindrical) Comsol simulation files.

Crystallographic data

Crystallographic cif file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.

Crystallographic data

Structure factors file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.

Crystallographic data

Structure factors file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morasch, M., Liu, J., Dirscherl, C.F. et al. Heated gas bubbles enrich, crystallize, dry, phosphorylate and encapsulate prebiotic molecules. Nat. Chem. 11, 779–788 (2019). https://doi.org/10.1038/s41557-019-0299-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41557-019-0299-5

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing