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Research Article

Origin of the RNA world: The fate of nucleobases in warm little ponds

View ORCID ProfileBen K. D. Pearce, Ralph E. Pudritz, Dmitry A. Semenov, and Thomas K. Henning
PNAS October 24, 2017 114 (43) 11327-11332; first published October 2, 2017; https://doi.org/10.1073/pnas.1710339114
Ben K. D. Pearce
aOrigins Institute, McMaster University, Hamilton, ON L8S 4M1, Canada;
bDepartment of Physics and Astronomy, McMaster University, Hamilton, ON L8S 4M1, Canada;
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  • ORCID record for Ben K. D. Pearce
  • For correspondence: pearcbe@mcmaster.ca
Ralph E. Pudritz
aOrigins Institute, McMaster University, Hamilton, ON L8S 4M1, Canada;
bDepartment of Physics and Astronomy, McMaster University, Hamilton, ON L8S 4M1, Canada;
cPlanet and Star Formation Department, Max Planck Institute for Astronomy, 69117 Heidelberg, Germany;
dInstitute for Theoretical Astrophysics, Center for Astronomy Heidelberg, 69120 Heidelberg, Germany
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Dmitry A. Semenov
cPlanet and Star Formation Department, Max Planck Institute for Astronomy, 69117 Heidelberg, Germany;
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Thomas K. Henning
cPlanet and Star Formation Department, Max Planck Institute for Astronomy, 69117 Heidelberg, Germany;
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  1. Edited by Donald E. Canfield, Institute of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M., Denmark, and approved August 28, 2017 (received for review June 7, 2017)

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Significance

There are currently two competing hypotheses for the site at which an RNA world emerged: hydrothermal vents in the deep ocean and warm little ponds. Because the former lacks wet and dry cycles, which are well known to promote polymerization (in this case, of nucleotides into RNA), we construct a comprehensive model for the origin of RNA in the latter sites. Our model advances the story and timeline of the RNA world by constraining the source of biomolecules, the environmental conditions, the timescales of reaction, and the emergence of first RNA polymers.

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.

  • life origins
  • astrobiology
  • planetary science
  • meteoritics
  • RNA world

Footnotes

  • ↵1To whom correspondence should be addressed. Email: pearcbe{at}mcmaster.ca.
  • Author contributions: B.K.D.P., R.E.P., D.A.S., and T.K.H. designed research; B.K.D.P. performed research; B.K.D.P. and R.E.P. analyzed data; and B.K.D.P., R.E.P., D.A.S., and T.K.H. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 11264.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1710339114/-/DCSupplemental.

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Fate of nucleobases in warm little ponds
Ben K. D. Pearce, Ralph E. Pudritz, Dmitry A. Semenov, Thomas K. Henning
Proceedings of the National Academy of Sciences Oct 2017, 114 (43) 11327-11332; DOI: 10.1073/pnas.1710339114

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Fate of nucleobases in warm little ponds
Ben K. D. Pearce, Ralph E. Pudritz, Dmitry A. Semenov, Thomas K. Henning
Proceedings of the National Academy of Sciences Oct 2017, 114 (43) 11327-11332; DOI: 10.1073/pnas.1710339114
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Proceedings of the National Academy of Sciences: 114 (43)
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Article Classifications

  • Physical Sciences
  • Earth, Atmospheric, and Planetary Sciences

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  • Article
    • Abstract
    • Model: Fates of Nucleobases in Evolving WLPs
    • SI Text
    • Calculating WLP Surface Area on Early Earth
    • Calculating Carbonaceous Meteorite Depositions in WLPs
    • Sources and Sinks Model Overview
    • Pond Water Sources and Sinks
    • Nucleobase Sinks
    • Nucleobase Outflow and Mixing
    • Nucleobase Evolution Equation from IDPs
    • Nucleobase Evolution Equation from Meteorites
    • Additional Results
    • Advection and Diffusion Model
    • Meteorite Sources and Targets
    • Life Cycles of WLPs
    • Nucleobase Evolution in WLPs
    • Dominant Source of Surviving Nucleobases
    • Nucleotide and RNA Synthesis
    • Discussion and Conclusions
    • Acknowledgments
    • Footnotes
    • References
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