Spontaneous network formation among cooperative RNA replicators (original) (raw)

Nature volume 491, pages 72–77 (2012)Cite this article

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Abstract

The origins of life on Earth required the establishment of self-replicating chemical systems capable of maintaining and evolving biological information. In an RNA world, single self-replicating RNAs would have faced the extreme challenge of possessing a mutation rate low enough both to sustain their own information and to compete successfully against molecular parasites with limited evolvability. Thus theoretical analyses suggest that networks of interacting molecules were more likely to develop and sustain life-like behaviour. Here we show that mixtures of RNA fragments that self-assemble into self-replicating ribozymes spontaneously form cooperative catalytic cycles and networks. We find that a specific three-membered network has highly cooperative growth dynamics. When such cooperative networks are competed directly against selfish autocatalytic cycles, the former grow faster, indicating an intrinsic ability of RNA populations to evolve greater complexity through cooperation. We can observe the evolvability of networks through in vitro selection. Our experiments highlight the advantages of cooperative behaviour even at the molecular stages of nascent life.

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Figure 1: Cooperative covalent assembly of recombinase ribozymes.

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Figure 2: Cooperative chemistry out-competes selfish chemistry when directly competed.

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Figure 3: The randomization experiment.

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Figure 4: The serial transfer experiment.

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Figure 5: Growth curve of a four-piece system.

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Change history

A minor typo in Fig. 1 was corrected.

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Acknowledgements

We would like to thank A. Burton, R. Ghadiri, P. Higgs, B. Larson, K. Chacón and A. López García de Lomana for help during preparation of this manuscript. This work was supported by NASA grant NNX10AR15G to N.L., the Center for Life in Extreme Environments at Portland State University, and a fellowship from the Human Frontier Science Program Organization to R.X.-B.

Author information

Author notes

  1. Irene A. Chen
    Present address: Present address: Department of Chemistry and Biochemistry, University of California, Santa Barbara, California 93106, USA.,

Authors and Affiliations

  1. Department of Chemistry, Portland State University, PO Box 751, Portland, Oregon 97207, USA,
    Nilesh Vaidya & Niles Lehman
  2. School of Engineering and Applied Sciences and Program for Evolutionary Dynamics, Harvard University, Cambridge, 02138, Massachusetts, USA
    Michael L. Manapat
  3. FAS Center for Systems Biology, Harvard University, Cambridge, 02138, Massachusetts, USA
    Irene A. Chen & Ramon Xulvi-Brunet
  4. Department of Bioengineering, Stanford University, Stanford, 94305, California, USA
    Eric J. Hayden

Authors

  1. Nilesh Vaidya
  2. Michael L. Manapat
  3. Irene A. Chen
  4. Ramon Xulvi-Brunet
  5. Eric J. Hayden
  6. Niles Lehman

Contributions

N.L. and N.V. conceived the basic idea and conducted the experiments; E.J.H. and I.A.C. contributed to the evaluation of the results; I.A.C., M.L.M. and R.X.-B. constructed the mathematical models; N.L. wrote the manuscript.

Corresponding author

Correspondence toNiles Lehman.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary Text and Data, a Supplementary Discussion, Supplementary Figures 1-14, Supplementary Tables 1-3 and additional references. (PDF 4848 kb)

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Vaidya, N., Manapat, M., Chen, I. et al. Spontaneous network formation among cooperative RNA replicators.Nature 491, 72–77 (2012). https://doi.org/10.1038/nature11549

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Comments

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  1. Mike Miller 31 March 2013, 11:07
    Thank you for an excellent article.
    The following comments pertain to the application of this study to abiogenesis:
    There are still several considerations before such an article should be cited as evidence for abiogenesis.
  1. Start with a pre-existing system, (The ~200-nucleotide (nt) Azoarcus group I intron ribozyme22 can be broken into fragments that can covalently self-assemble by catalysing recombination reactions in an autocatalytic fashion.
    I'm sure someone will cite this as evidence of complex systems originating from simpler systems thus making abiogenesis appear as a sound scientific theory. Wait, what; they took an enzyme and fragmented it, and then noticed that many of the components have a similar function.... Is that similar to several indistinct components spontaneously forming and then organizing into a system that forms an enzyme? Not to mention the lack of thermocycler etc. Not to mention that these sequences do not even code for any proteins, which are hundreds of amino acids in length, and just by chance happen to have relevant cellular functions, and happen to be assembled with the adjunct of chaperones; and happen to facilitate the production of a membrane with modified lipids and integral proteins. In summary, abiogenesis remains as tangible as a man getting safely to the moon after being stranded on a desert island.

Editorial Summary

Cooperativity in an RNA world

In models of early life characterized by an RNA-only world, it has been suggested that life and evolution would be more easily achieved if the RNA molecules could interact, rather than function independently. They can. Niles Lehman and colleagues demonstrate the validity of the concept in vitro using a model system containing RNA fragments that can assemble into a ribozyme. The authors show that the cooperative networks formed by these fragments can outcompete self-catalytic RNA fragments. This work indicates that RNA populations have an intrinsic ability to evolve greater complexity through cooperation, and suggests that the benefits of such behaviour were established early in the development of life on Earth.

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