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
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
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
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
Schrödinger, E. What is Life? The Physical Aspect of the Living Cell (Cambridge Univ. Press, 1944).
Cross, M. C. & Hohenburg, P. Pattern-formation outside of equilibrium. Rev. Mod. Phys. 65, 851–1112 (1993).
Bodenschatz, E., Pesch, W. & Ahlers, G. Recent developments in Rayleigh–Benard convection. Annu. Rev. Fluid Mech. 32, 709–778 (2000).
Fritts, D. C. & Alexander, M. J. Gravity wave dynamics and effects in the middle atmosphere. Rev. Geophys. 41, 1003 (2003).
Eaton, J. K. & Fessler, J. R. Preferential concentration of particles by turbulence. Int. J. Multiph. Flow 20, 169–209 (1994).
Götzendorfer, A., Kruelle, C. A., Rehberg, I. & Svenšek, D. Localized subharmonic waves in a circularly vibrated granular bed. Phys. Rev. Lett. 97, 198001 (2006).
Chen, J. & Lopez, J. A. Interactions of platelets with subendothelium and endothelium. Microcirculation 12, 235–246 (2005).
Moore, W. B. & Webb, A. A. G. Heat-pipe Earth. Nature 501, 501–505 (2013).
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).
Duhr, S. & Braun, D. Why molecules move along a temperature gradient. Proc. Natl Acad. Sci. USA 103, 19678–19682 (2006).
Baaske, P. et al. Extreme accumulation of nucleotides in simulated hydrothermal pore systems. Proc. Natl Acad. Sci. USA 104, 9346–9351 (2007).
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).
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).
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).
Morasch, M., Braun, D. & Mast, C. B. Heat-flow-driven oligonucleotide gelation separates single-base differences. Angew. Chem. Int. Ed. 55, 6676–6679 (2016).
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).
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).
Lerman, L. Potential role of bubbles and droplets in primordial and planetary chemistry. Orig. Life Evol. Biosph. 16, 201–202 (1986).
Ariga, K. & Hill, J. P. Monolayers at air–water interfaces: from origins-of-life to nanotechnology. Chem. Rec. 11, 199–211 (2011).
Eickbush, T. H. & Moudrianakis, E. N. A mechanism for the entrapment of DNA at an air–water interface. Biophys. J. 18, 275–288 (1977).
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).
Deegan, R. D. et al. Capillary flow as the cause of ring stains from dried liquid drops. Nature 389, 827–829 (1997).
Smith, K. A. On convective instability induced by surface-tension gradients. J. Fluid Mech. 24, 401–414 (1966).
Batchelor, G. K. An Introduction to Fluid Dynamics (Cambridge Univ. Press, 1973).
Deegan, R. D. Pattern formation in drying drops. Phys. Rev. E 61, 475–485 (2000).
Larson, R. G. Transport and deposition patterns in drying sessile droplets. AIChE J. 60, 1538–1571 (2014).
Savino, R., Paterna, D. & Favaloro, N. Buoyancy and marangoni effects in an evaporating drop. J. Thermophys. Heat Transf. 16, 562–574 (2002).
Drobot, B. et al. Compartmentalised RNA catalysis in membrane-free coacervate protocells. Nat. Commun. 9, 3643 (2018).
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).
Dahm, S. C. & Uhlenbeck, O. C. Role of divalent metal ions in the hammerhead RNA cleavage reaction. Biochemistry 30, 9464–9469 (1991).
Zhu, T. F. & Szostak, J. W. Coupled growth and division of model protocell membranes. J. Am. Chem. Soc. 131, 5705–5713 (2009).
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).
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).
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).
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).
Jones, S. F., Evans, G. M. & Galvin, K. P. Bubble nucleation from gas cavities—a review. Adv. Colloid Interface Sci. 80, 27–50 (1999).
Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239–242 (2009).
Lohrmann, R. & Orgel, L. E. Urea–inorganic phosphate mixtures as prebiotic phosphorylating agents. Science 171, 490–494 (1971).
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).
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).
Sosson, M. & Richter, C. Enzyme-free genetic copying of DNA and RNA sequences. Beilstein J. Org. Chem. 14, 603–617 (2018).
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).
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).
Vaidya, N. et al. Spontaneous network formation among cooperative RNA replicators. Nature 491, 72–77 (2012).
Mutschler, H., Wochner, A. & Holliger, P. Freeze–thaw cycles as drivers of complex ribozyme assembly. Nat. Chem. 7, 502–508 (2015).
Soukup, G. A. & Breaker, R. R. Relationship between internucleotide linkage geometry and the stability of RNA. RNA 5, 1308–1325 (1999).
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).
Rajmani, S. et al. Lipid-assisted synthesis of RNA-like polymers from mononucleotides. Orig. Life Evol. Biosph. 38, 57–74 (2008).
Reineck, P., Wienken, C. J. & Braun, D. Thermophoresis of single stranded DNA. Electrophoresis 31, 279–286 (2010).
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).
Lide, D. R. CRC Handbook of Chemistry and Physics (CRC Press, 2001).
Li, Y. & Gregory, S. Diffusion of ions in sea water and in deep-sea sediments. Geochim. Cosmochim. Acta 33, 703–714 (1974).
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).
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
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
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41557-019-0299-5
This article is cited by
-
Biogeochemical explanations for the world’s most phosphate-rich lake, an origin-of-life analog
Communications Earth & Environment (2024)
-
Multicompartmental coacervate-based protocell by spontaneous droplet evaporation
Nature Communications (2024)
-
Ribozyme-mediated RNA synthesis and replication in a model Hadean microenvironment
Nature Communications (2023)
-
Periodic temperature changes drive the proliferation of self-replicating RNAs in vesicle populations
Nature Communications (2023)
-
Physical non-equilibria for prebiotic nucleic acid chemistry
Nature Reviews Physics (2023)