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Heat flows in rock cracks naturally optimize salt compositions for ribozymes

An Author Correction to this article was published on 09 September 2021

This article has been updated


Catalytic nucleic acids, such as ribozymes, are central to a variety of origin-of-life scenarios. Typically, they require elevated magnesium concentrations for folding and activity, but their function can be inhibited by high concentrations of monovalent salts. Here we show that geologically plausible high-sodium, low-magnesium solutions derived from leaching basalt (rock and remelted glass) inhibit ribozyme catalysis, but that this activity can be rescued by selective magnesium up-concentration by heat flow across rock fissures. In contrast to up-concentration by dehydration or freezing, this system is so far from equilibrium that it can actively alter the Mg:Na salt ratio to an extent that enables key ribozyme activities, such as self-replication and RNA extension, in otherwise challenging solution conditions. The principle demonstrated here is applicable to a broad range of salt concentrations and compositions, and, as such, highly relevant to various origin-of-life scenarios.

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Fig. 1: Schematic diagrams of the proposed prebiotic scenario and the experimental set-up.
Fig. 2: Leaching of salts from basaltic rock.
Fig. 3: Thermal microfluidic set-up and numerical control.
Fig. 4: Influence of salt conditions and thermal trapping on a replicator ribozyme ER and a ladder-building ribozyme EL.
Fig. 5: Interconnected channels in a basaltic complex allow a variety of possible salt conditions.

Data availability

The data supporting the findings of this study are available within the paper and its Supplementary Information. Raw data in the form of images (gels) or data series (Excel files) are also provided in the Supplementary Information. Source data are provided with this paper.

Code availability

The full details of the finite element simulation from Fig. 3 are documented in the mph files in the Supplementary Information. The extrapolation from Fig. 5d,e and Supplementary Figs. 1419 was done using a Labview program, which is also provided in the Supplementary Source file.

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Funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)—Project-ID 364653263–TRR 235 (CRC235), Project P08 (C.B.M. and H.M.), P09 (D.B. and B.S.) and P03 (B.S.). Funding by the Volkswagen Initiative ‘Life?—A Fresh Scientific Approach to the Basic Principles of Life’ (C.B.M., D.B., H.M., K.L.V., T.M., D.B.D. and A.Z.Ç.), from the Simons Foundation (327125 to D.B.) and from Germany’s Excellence Strategy EXC-2094-390783311 is gratefully acknowledged. We thank Quantitative Biology Munich for funding (A.K.). This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 802000, RiboLife) (H.M.). H.M. is grateful for funding by the MaxSynBio consortium, which is jointly funded by the Federal Ministry of Education and Research of Germany and the Max Planck Society. D.B.D. acknowledges the support of ERC ADV 2018 Grant 834225 (EAVESDROP) and D.B. is grateful for financial support from ERC-2017-ADG from the European Research Council. The work is supported by the Center for Nanoscience Munich (CeNS). We thank E. Song for fruitful discussions.

Author information

Authors and Affiliations



T.M., K.L.V., A.S., P.A., L.B., A.Z.Ç., E.S., C.S. and C.B.M. performed the experiments. T.M., K.L.V., A.S., L.B., A.Z.Ç., E.S., A.K., C.S., B.S., D.B.D., D.B., H.M. and C.B.M. conceived and designed the experiments. T.M., K.L.V., P.A., L.B., A.Z.Ç., E.S., A.K., C.S., B.S., H.M. and C.B.M. analysed the data. T.M., K.L.V., A.S., P.A., L.B., A.Z.Ç., A.K., B.S., D.B., H.M. and C.B.M. wrote the paper. All the authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to H. Mutschler or C. B. Mast.

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The authors declare no competing interests.

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Peer review information Nature Chemistry thanks Katarzyna Adamala, Rowena Ball and Philip Bevilacqua for their contribution to the peer review of this work.

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

Extended data

Extended Data Fig. 1 Leaching of salts from basaltic rock and glass.

Except where stated otherwise, 30 mg of sample were leached at 60 °C in 150 µl ultrapure water without agitation. (a) Tholeiite glass samples with grain size of 90-125 µm and a weight of up to 120 mg were leached at 60 °C in 150 µl pure water for 110 h. Magnesium and calcium concentrations remain at similarly low levels (200 µM), while sodium concentration exceeds by up to a factor of three. Standard deviations are taken from g, grain size 90-125 µm. (b) Tholeiite rock samples of 90-125 µm size were leached for 36 h under the same conditions as in a. Error bars are taken from e. (c) Characteristic equilibration timescales for tholeiite glass, as shown for magnesium in the main text, Fig. 2. Timescales are around 30 hours. The grain size used here is 355-500 µm. For comparison with e, the leached concentrations are converted to 90-125 µm grains using the grain size dependence from g. (d) Grain size dependence of leached salt concentrations for tholeiite glass, incubated at 60 °C for 95 h. (e) Characteristic equilibration timescales for basaltic rock of grain size 90-125 µm under the same conditions as in d. (f) Complete picture of leached ions from tholeiite glass (grain size 125-180 µm, 110 h, 60 °C, pure water). In the first place, sodium (120 µM) is leached with magnesium and calcium (both 90 µM) following at lower concentrations. Fluoride, chloride and potassium are detectable at low concentrations (all 10-20 µM). Other trace elements such as phosphate, nitrite and nitrate are present but below 2 µM. (g) Basalt glass samples of 355-500 µm grain size were leached for 48 h at varying temperature under otherwise identical conditions as in a. The leached salt concentrations increase with temperature but stay at low levels.

Source data

Extended Data Fig. 2 Detailed description of fluidic setup.

(a) Fluidic setup. Microfluidic access to the heat flow cell is implemented by backside connection of FEP tubing through the four access holes on the backside aluminium and sapphire pieces (see Supplementary Fig. 2). Slow geothermal convection is mimicked by a slow through flow, controlled by three high precision syringe pumps with a constant volume rate. One pump (in) provides positive pressure and injects fresh sample into the chamber. The remaining two pumps (top, bot) provide negative pressure and remove the sample from the top or bottom output, respectively. The centered output (mid) releases the remaining pressure to an open Eppendorf tube. To minimized possible detrimental surface interactions, the complete system including chamber, tubing and syringes is pre-flushed with fluorinated oil. After the experiment, samples from bot, mid and top are recovered from the tubing and analyzed via IC. (b) Optothermal setup. Special care was taken to precisely determine the temperature inside the microfluidic layer: A temperature sensor is directly in contact with the cold sapphire from the backside and held in place via a UNF screw (grey). The surface temperature of the hot sapphire is measured with an IR camera (IR). The temperature field inside the liquid is then calculated from the known heat conductivity of the sapphire layers. Fluorescence measurements of the RNA reaction were obtained using a custom-made, motorized fluorescence microscope comprising an objective (O, TL4/2X-SAP, Thorlabs), dichroic mirror (M), excitation and emission filters (XF, EF, Cy5 Kit XF416, Laser Components), a lens (L) that collimates the light from a LED (LED, M625L3, Thorlabs) and a camera (C, Stingray 145-B, Allied Vision).

Extended Data Fig. 3 Thermal design of the heat flow cell using finite element simulations.

(a) The full three-dimensional model including all elements shown in Supplementary Fig. 2. The temperature was measured on the cold aluminum base and on the heating element by thermistors and kept constant under PID control. The temperatures on the hot and cold sapphire are measured with an IR camera and a thermistor (S), respectively, and compared to the calculated 2D temperature distribution. Thus, the temperature distribution on the cold or hot side within the microfluidic chamber can be derived. (b) The two-dimensional average of a depicts the calculated temperature distribution on the z-y surface in the center of the chamber, showing the uniform temperature distribution along the y-axis. (c) One-dimensional average of b. Most of the temperature difference is effective in the microfluidic chamber filled with aqueous solution.

Extended Data Fig. 4 Trapping experiments with other salt species and control.

Errors bars represent the standard deviation calculated from data provided in Supplementary Table 3. (a) Selective accumulation of sodium, potassium, magnesium and calcium. In an experiment similar to Fig. 3, main text, samples of 1.5 mM of all salts were pushed through the microfluidic chamber at 11.8 nl/s applying a temperature gradient of 40 K to analyze selective accumulation. As shown, sodium (2.3-fold) and potassium (2-fold) are less accumulated at the bottom than magnesium (3.4-fold) and calcium (4.5-fold). Together with a top outlet that is mainly depleted in the latter but also has reduced concentration of Na and K, this opens the door to many different salty habitats. (b) Control experiments with no applied temperature gradient show (as expected) no shift of salt concentrations.

Source data

Extended Data Fig. 5 Secondary structure diagrams of ribozymes.

Diagrams showing the initial (a) and final (b) concatemer ligation ribozyme designs. In the initial design a, regions of the substrate originating from R3C substrate A are shown in red, whilst regions originating from substrate B are shown in blue. In b, mutations made to reduce homodimer formation and promote substrate binding are highlighted in pink.

Extended Data Fig. 6 Interconnected molecular traps mimicking branching rock fissures.

(a) Illustration of the system of interconnected molecular traps mimicking branching rock fissures in a realistic geological scenario. For a detailed description, see Supplementary Method 12 and Supplementary Figs. 1319. (b) Statistics of the accumulated concentrations at the chamber bottom for different temperature differences. Histogram of resulting ion concentrations. With increasing temperature difference, magnesium ions (orange) are increasingly better accumulated, up to 4 orders of magnitude better than sodium ions (blue) at ΔT=40 K. (c) Correlation plot for magnesium and sodium concentrations. At higher temperature differences, magnesium is accumulated with increasing selectivity compared to sodium. (d) Scaling of the width of the chamber system. Histogram of the frequency of chambers with a given concentration of magnesium (top) and sodium ions (bottom) at the chamber bottom for different temperature gradients ΔT=10 K (blue) and 30 K (red) and system widths \({{{\mathrm{N}}}}_{{{\mathrm{x}}}} = 25,\,50,\,100\) chambers. (e) Correlation plots of magnesium and sodium ion concentration at the chamber bottom at ΔT=10 K (top) and 30 K (bottom).

Source data

Supplementary information

Supplementary Information

Contains Supplementary text, figures, tables and source images for gels.

Supplementary Data 1

Contains all source data used in Graphs in the Supplementary Information.

Supplementary Software 1

Simulation file used in Fig. 3c / Main-Text.

Supplementary Software 2

Custom-made software and simulation file used to obtain Supplementary Figures 14–19.

Source data

Source Data Fig. 1

Contains source data to obtain Figure 1b.

Source Data Fig. 2

Source data for all shown graphs.

Source Data Fig. 3

Source data for Fig. 3b/c.

Source Data Fig. 4

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Source Data Fig. 4

Source images for gels Fig. 4c/h.

Source Data Fig. 5

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Source Data Extended Data Fig. 1

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Source Data Extended Data Fig. 4

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Source Data Extended Data Fig. 6

Source data for all shown graphs.

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Matreux, T., Le Vay, K., Schmid, A. et al. Heat flows in rock cracks naturally optimize salt compositions for ribozymes. Nat. Chem. 13, 1038–1045 (2021).

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