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Light-driven eco-evolutionary dynamics in a synthetic replicator system

Nature Chemistry volume 16, pages 79–88 (2024)Cite this article

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Abstract

Darwinian evolution involves the inheritance and selection of variations in reproducing entities. Selection can be based on, among others, interactions with the environment. Conversely, the replicating entities can also affect their environment generating a reciprocal feedback on evolutionary dynamics. The onset of such eco-evolutionary dynamics marks a stepping stone in the transition from chemistry to biology. Yet the bottom-up creation of a molecular system that exhibits eco-evolutionary dynamics has remained elusive. Here we describe the onset of such dynamics in a minimal system containing two synthetic self-replicators. The replicators are capable of binding and activating a co-factor, enabling them to change the oxidation state of their environment through photoredox catalysis. The replicator distribution adapts to this change and, depending on light intensity, one or the other replicator becomes dominant. This study shows how behaviour analogous to eco-evolutionary dynamics—which until now has been restricted to biology—can be created using an artificial minimal replicator system.

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Fig. 1: Self-replication, co-factor activation and rudimentary eco-evolutionary dynamics.
Fig. 2: Characterization of replicator 13.
Fig. 3: The oxidation level of the solution controls the outcome of replicator competition.
Fig. 4: Cross-catalysis between replicators 13 and 16.
Fig. 5: Replicator-mediated activation of co-factor 2 and photocatalytic self-replication.
Fig. 6: Eco-evolutionary dynamics involving replicator-induced changes in the oxidation level of the environment that, in turn, cause evolutionary changes to the replicator mutant distribution.

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Data availability

The UPLC data generated and analysed in this article are included in its Supplementary Information in the form of integrated peak areas and exported traces of representative chromatograms. All other data generated or analysed during this study are included in this published article and its Supplementary Information. Waters UPLC software stores raw UPLC data in a database format from which they are not readily extractable. These data are available on request. Source data are provided with this paper.

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Acknowledgements

The authors thank W. R. Browne (University of Groningen) for the phosphorescence and EPR measurements and O. Markovitch (University of Groningen) for providing guidance on the usage of UPLC stirring device. This work was supported by the Simons Foundation (553330; K.L.), Marie Curie Individual Fellowships (PSR 786350; K.L.), the oLife Cofund programme (847675; A.B.), the ERC (AdG 741774), the China Scholarship Council (J.W.) and the Dutch Ministry of Education, Culture and Science (Gravitation programme 024.001.035; A.K. and S.O.).

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Authors and Affiliations

  1. Centre for Systems Chemistry, Stratingh Institute, University of Groningen, Groningen, the Netherlands

    Kai Liu, Alex Blokhuis, Armin Kiani, Juntian Wu & Sijbren Otto

  2. Molecular Biophysics, Zernike Institute for Advanced Materials, University of Groningen, Groningen, the Netherlands

    Chris van Ewijk & Wouter H. Roos

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Contributions

K.L. and S.O. conceived the concept. K.L. designed, performed experiments and analysed the data. A.B. assisted in the data analysis and contributed to the scientific discussion. C.E. performed the experiments related to HS-AFM. C.E. and W.H.R. analysed the data related to HS-AFM. A.K. performed the experiments related to TEM. J.W. performed the experiments related to UPLC–MS. K.L. A.B. and S.O. wrote the manuscript.

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Correspondence to Sijbren Otto.

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Nature Chemistry thanks David Lynn, Subhabrata Maiti and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–58 and Tables 1 and 2.

Supplementary Video 1

HS-AFM showing the growth of 3-mer fibres from the ends liberated by fibre breakage.

Supplementary Video 2

HS-AFM showing the growth of a single 3-mer fibre.

Source data

Source Data Fig. 2

Relative peak area of components in the sample obtained from UPLC chromatograms.

Source Data Fig. 3

Relative/absolute peak areas of components in the sample obtained from UPLC chromatograms; calculation of the relative change of the peak areas, the concentration of bound precursor, the adsorption efficiency, and replication rate.

Source Data Fig. 4

Relative peak areas of components in the sample obtained from UPLC chromatograms.

Source Data Fig. 5

Raw spectral data; absolute peak areas of the monomer in UPLC chromatograms, and calculation of oxidation rates from them; Relative peak areas of components in the sample obtained from UPLC chromatograms.

Source Data Fig. 6

Relative peak areas of components in the sample in UPLC chromatograms.

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Liu, K., Blokhuis, A., van Ewijk, C. et al. Light-driven eco-evolutionary dynamics in a synthetic replicator system. Nat. Chem. 16, 79–88 (2024). https://doi.org/10.1038/s41557-023-01301-2

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