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. 2017 Oct 24;114(43):11327-11332.
doi: 10.1073/pnas.1710339114. Epub 2017 Oct 2.

Origin of the RNA World: The Fate of Nucleobases in Warm Little Ponds

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Free PMC article

Origin of the RNA World: The Fate of Nucleobases in Warm Little Ponds

Ben K D Pearce et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Before the origin of simple cellular life, the building blocks of RNA (nucleotides) had to form and polymerize in favorable environments on early Earth. At this time, meteorites and interplanetary dust particles delivered organics such as nucleobases (the characteristic molecules of nucleotides) to warm little ponds whose wet-dry cycles promoted rapid polymerization. We build a comprehensive numerical model for the evolution of nucleobases in warm little ponds leading to the emergence of the first nucleotides and RNA. We couple Earth's early evolution with complex prebiotic chemistry in these environments. We find that RNA polymers must have emerged very quickly after the deposition of meteorites (less than a few years). Their constituent nucleobases were primarily meteoritic in origin and not from interplanetary dust particles. Ponds appeared as continents rose out of the early global ocean, but this increasing availability of "targets" for meteorites was offset by declining meteorite bombardment rates. Moreover, the rapid losses of nucleobases to pond seepage during wet periods, and to UV photodissociation during dry periods, mean that the synthesis of nucleotides and their polymerization into RNA occurred in just one to a few wet-dry cycles. Under these conditions, RNA polymers likely appeared before 4.17 billion years ago.

Keywords: RNA world; astrobiology; life origins; meteoritics; planetary science.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. S6.
Fig. S6.
The dotted circle represents the target area for landing the dispersed fragments from a single meteoroid into any WLP on early Earth. The smaller, light gray circle in the center is the total combined WLP surface area on early Earth at a given time (WLPs would have been individually scattered; however, for a geometric probability calculation, they can be visualized as a single pond cross-section). The larger, surrounding circles represent the area of debris when the fragments of the meteoroid hit the ground. Shortly after 4.5 Ga, the area of debris from a single meteoroid would be large compared with the combined WLP surface area. At any time, the target area for a meteoroid to deposit fragments homogeneously into at least one WLP is slightly larger than the combined area of WLPs. The effective target area grows linearly with total WLP surface area. The diagonally striped intersections between the circles represent the largest individual WLP for which the meteoroid fragment deposition probability is being calculated. The logic is that, if a meteoroid enters the atmosphere at distance d from the center of the combined pond cross-section, at least one pond of any size in the WLP distribution will completely overlap with the area of debris.
Fig. S7.
Fig. S7.
Normalized probability distributions of fragments from CM-, CI-, and CR-type meteoroids with radii 20 m to 40 m landing in WLPs on early Earth of radii 1 m to 10 m. Three models for mass delivery are compared: the LHB model, and minimum and maximum mass models for a sustained, declining bombardment preceding 3.9 Ga. All models are based on analyses of the lunar cratering record (6, 21). See Fig. 1 for display of mass delivery rates. The 95% confidence intervals are shaded, and correspond to the most likely deposition intervals for each model.
Fig. S8.
Fig. S8.
The nucleobase mixing time in a base-to-surface convection cell (length = 2rp) within 1-, 5-, and 10-m-deep WLPs, beginning from a local concentration at the base of the pond. Nucleobase mixing is measured using the maximum percent local nucleobase concentration difference from the average. The time at which the maximum local nucleobase concentration difference from the average drops to 10% is labeled on the plot for each pond size. At this time, we consider the nucleobases in the WLP to be well mixed. For WLPs with radii 1, 5, and 10 m, the convection cell nucleobase mixing times are 35, 104, and 150 min, respectively.
Fig. S9.
Fig. S9.
The effect of temperature on the change in water mass over time in wet environment cylindrical WLPs with radii and depths of 1 m. Temperatures are varied for a hot early Earth model (50 °C, 65 °C, and 80 °C) and a warm early Earth model (5 °C, 20 °C, and 35 °C). Precipitation rates from Columbia and Thailand on Earth today are used to represent the hot and warm early Earth analogues, respectively (for details, see Table 1). COL, Columbia; THA, Thailand.
Fig. S10.
Fig. S10.
The accumulation of adenine from 1-cm fragments of an initially 40-m-radius carbonaceous meteoroid in a cylindrical WLP with a radius and depth of 1 m. The degenerate WLP models used for these calculations correspond to a hot early Earth at 65 °C and a warm early Earth at 20 °C. (A) The accumulation of adenine from carbonaceous meteorites in an intermediate environment (for details, see Table 1). The wet–dry cycles of the pond are also shown to illustrate the effect of water level on adenine concentration. (B) The three curves (dry, intermediate, and wet environments) differ by their precipitation rates, which are from a variety of locations on Earth today, and represent two classes of matching early Earth analogues: hot (Columbia, Indonesia, Cameroon) and warm (Thailand, Brazil, and Mexico) (for details, see Table 1). The curves are obtained by numerically solving Eq. S38. BRA, Brazil; Env, environment; IDN, Indonesia.
Fig. S11.
Fig. S11.
The maximum concentration of adenine accumulated from 1-cm fragments of a carbonaceous meteoroid 20 m to 40 m in radius in cylindrical WLPs with radii and depths of 1 m. The degenerate WLP models used for these calculations correspond to a hot early Earth at 65 °C and a warm early Earth at 20 °C. The three curves (dry, intermediate, and wet environments) differ by their precipitation rates, which are from a variety of locations on Earth today, and represent two classes of matching early Earth analogues: hot (Columbia, Indonesia, Cameroon) and warm (Thailand, Brazil, and Mexico) (for details, see Table 1). The curves are obtained by numerically solving Eq. S38. Env, environment.
Fig. S12.
Fig. S12.
Example simulations, including the initial conditions, for our two-part nucleobase transport model. Each line represents a different snapshot in time. (A) Initially homogeneous nucleobase diffusion from a 100-μm-radius carbonaceous IDP. (B) Initially locally concentrated nucleobase mixing in a convection cell within a 1-m-deep WLP. The convection cell is an L = 2rp eccentric loop flowing between the bottom and the top of the WLP. This loop is sliced at r = 1 m in the convection cell’s moving frame and unraveled for display in the 1D plot in B.
Fig. 1.
Fig. 1.
History of carbonaceous meteorite deposition in WLPs. (A) History of mass delivery rate to early Earth and of effective WLP surface area. Three models for mass delivered to early Earth are compared: an LHB model and a minimum and a maximum bombardment model. All mass delivery models are based on analyses of the lunar cratering record (6, 21). The effective WLP surface area during the Hadean Eon is based on a continental crust growth model (29), the number of lakes and ponds per unit crustal area (23), and the lake and pond size distribution (23). (B) Cumulative WLP depositions for the small fragments of carbonaceous meteoroids of diameter 40 m to 80 m landing in any 1- to 10-m-radius WLP on early Earth. A deposition is characterized as a meteoroid debris field that overlaps with a WLP. We assume the ponds per area during the Hadean Eon is the same as today, and that all continental crust remains above sea level; however, we vary the ponds per area by plus or minus one order of magnitude to obtain error bars. Ninety-five percent of WLP depositions in each model occur before the corresponding dotted vertical line; 40 m to 80 m is the optimal range of carbonaceous meteoroid diameters to reach terminal velocity, while still landing a substantial fraction of mass within a WLP area; and 1 m to 10 m is the optimal range of WLP radii to avoid complete evaporation within a few months, while also allowing nonnegligible nucleobase concentrations to be reached upon meteorite deposition. The numbers of carbonaceous meteoroid impactors in the 20- to 40-m-radius range are based on the mass delivery rate, the main-belt size-frequency distribution, and the fraction of impactors that are Mighei type, Renazzo type, or Ivuna type (6, 21, 22) (see SI Text).
Fig. 2.
Fig. 2.
An illustration of the sources and sinks of pond water and nucleobases in our model of isolated WLPs on early Earth. The only water source is precipitation. Water sinks include evaporation and seepage. Nucleobase sources include carbonaceous IDPs and meteorites, which carry up to 1 pg and 3 mg, respectively, of each nucleobase. Nucleobase sinks include hydrolysis, UV photodissociation, and seepage. Nucleobase hydrolysis and seepage are only activated when the pond is wet, and UV photodissociation is only activated when the pond is dry.
Fig. 3.
Fig. 3.
Histories of pond water and adenine concentration from IDPs. (A) The change in water level over time in our fiducial dry, intermediate, and wet environment WLPs due to evaporation, seepage, and precipitation. Precipitation rates from a variety of locations on Earth today are used in the models, and represent two classes of matching early Earth analogues: hot (Columbia, Indonesia, Cameroon) and warm (Thailand, Brazil, and Mexico) (for details, see Table 1). All models begin with an empty pond, and stabilize within 2 y. (B) The red and black-dotted curves represent the adenine concentrations over time from carbonaceous IDPs in our fiducial WLPs. The degenerate intermediate WLP environment used in this calculation is for a hot early Earth at 65 °C and a warm early Earth at 20 °C. The blue curve represents the corresponding water level in the WLP, with initial empty and full states labeled vertically. Three features are present: (1) the maximum adenine concentration at the onset of the dry phase, (2) a flat-top equilibrium between incoming adenine from IDPs and adenine destruction by UV irradiation, and (3) the minimum adenine concentration just before the pond water reaches its highest level. BRA, Brazil; CAM, Cameroon; COL, Columbia; Env, environment; IDN, Indonesia; MEX, Mexico; THA, Thailand.
Fig. S1.
Fig. S1.
The accumulation of adenine from only carbonaceous IDP sources in cylindrical WLPs with radii and depths of 1 m. The three curves (dry, intermediate, and wet environments) differ by their precipitation rates, which are from a variety of locations on Earth today, and represent two classes of matching early Earth analogues: hot (Columbia, Indonesia, Cameroon) and warm (Thailand, Brazil, and Mexico) (for details see Table 1). (A) The degenerate WLP models used for these calculations correspond to a hot early Earth at 65 °C and a warm early Earth at 20 °C. (B) The degenerate WLP models used for these calculations correspond to a hot early Earth at 50 °C and a warm early Earth at 5 °C. Env, environment.
Fig. 4.
Fig. 4.
Comparative histories of adenine concentrations from IDPs and meteorites. (A) A comparison of the accumulation of adenine from carbonaceous IDPs and meteorites in our fiducial WLPs. The meteorite fragments are small (1 cm), and originate from a 40-m-radius carbonaceous meteoroid. Adenine concentrations for intermediate (wet–dry cycle) and wet environments (never dry) are compared and correspond to both a hot early Earth at 65 °C and a warm early Earth at 20 °C (for details, see Table 1). (B) The effect of meteorite fragment sizes on adenine concentration. The degenerate intermediate WLP environment used in these calculations is for a hot early Earth at 65 °C and a warm early Earth at 20 °C. The fragments are either only small in size (1 cm in radius), only medium in size (5 cm in radius), or only large in size (10 cm in radius). Three features are present: (1) Adenine is at its highest concentration at the onset of the pond’s dry phase. (2) Upon drying, adenine ceases to outflow from large fragments, and UV radiation rapidly destroys all previously released adenine. (3) Rewetting allows the remaining adenine within large fragment pores to continue to outflow. The U shape is due to the increase and decrease in water level. Env, environment.
Fig. S2.
Fig. S2.
The accumulation of guanine, adenine, uracil, and cytosine from only carbonaceous IDP sources in cylindrical WLPs with radii and depths of 1 m. The degenerate dry WLP models used for these calculations correspond to a hot early Earth at 65 °C and a warm early Earth at 20 °C. Precipitation rates from Cameroon and Mexico on Earth today are used to represent the hot and warm early Earth analogues, respectively (for details, see Table 1). The cytosine abundance in IDPs used to calculate the maximum cytosine curve matches the average abundance of guanine in IDPs (Table S2). The curves are obtained by numerically solving Eq. S34.
Fig. S3.
Fig. S3.
The accumulation of guanine, adenine, and uracil from 1-cm fragments of an initially 40-m-radius carbonaceous meteoroid in cylindrical WLPs with radii and depths of 1 m. The degenerate WLP models used for these calculations correspond to a hot early Earth at 65 °C and a warm early Earth at 20 °C. The two curves for each nucleobase differ by their precipitation rates, which create intermediate (solid lines) and wet (dotted lines) environments, and are from a variety of locations on Earth today, representing two classes of matching early Earth analogues: hot (Columbia, Indonesia) and warm (Thailand, Brazil) (for details, see Table 1). The curves are obtained by numerically solving Equation S38. Env, environment.
Fig. S4.
Fig. S4.
Fraction of the total initial nucleobases remaining in (A) a 100-μm-radius IDP and (B) 1-, 5-, and 10-cm-radii meteorites over time as a result of diffusion across a rock–pond boundary. The IDP and meteorites are considered to be lying on the bottom of a WLP, and are diffusing nucleobases symmetrically in the radial direction. The times at which 99% of the initial contained nucleobases have diffused into the WLP are labeled on the plots.
Fig. S5.
Fig. S5.
The no seepage limit: the accumulation of adenine from only carbonaceous IDP sources in cylindrical WLPs with radii and depths of 1 m. The two curves represent the adenine concentrations in a wet environment pond on a hot (65 °C) and warm (20 °C) early Earth (for details, see Table 1). The thickness of the lines is due to the seasonal oscillations in adenine concentrations. Env, environment.

Comment in

  • Darwin's prescient guess.
    Deamer D. Deamer D. Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):11264-11265. doi: 10.1073/pnas.1715433114. Epub 2017 Oct 13. Proc Natl Acad Sci U S A. 2017. PMID: 29073040 Free PMC article. No abstract available.

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