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.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $13.33 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
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.
The complete details of both simulations are documented in the html report and mph simulation files in the Supplementary Information.
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).
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.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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 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 Video 2 shows the accumulation of the Hammerhead ribozyme at the interface.
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.
In Supplementary Video 4, 100 nm oleic acid vesicles were accumulated together with a 72mer DNA at the interface.
Supplementary Video 5 shows a small bubble in a 150 µm-thick chamber filled with RAO.
Supplementary Video 6 shows the accumulation inside a bubble at a temperature gradient of 20 °C.
The Simulation File contains both the upright (Cartesian) as well as horizontally aligned (cylindrical) Comsol simulation files.
Crystallographic cif file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.
Structure factors file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.
Structure factors file for d-ribofuranosyl aminooxazoline; CCDC reference 1847429.
About this article
Emerging Topics in Life Sciences (2019)