Small-molecule autocatalysis drives compartment growth, competition and reproduction.
Journal
Nature chemistry
ISSN: 1755-4349
Titre abrégé: Nat Chem
Pays: England
ID NLM: 101499734
Informations de publication
Date de publication:
07 Aug 2023
07 Aug 2023
Historique:
received:
09
02
2022
accepted:
16
06
2023
medline:
8
8
2023
pubmed:
8
8
2023
entrez:
7
8
2023
Statut:
aheadofprint
Résumé
Sustained autocatalysis coupled to compartment growth and division is a key step in the origin of life, but an experimental demonstration of this phenomenon in an artificial system has previously proven elusive. We show that autocatalytic reactions within compartments-when autocatalysis, and reactant and solvent exchange outpace product exchange-drive osmosis and diffusion, resulting in compartment growth. We demonstrate, using the formose reaction compartmentalized in aqueous droplets in an emulsion, that compartment volume can more than double. Competition for a common reactant (formaldehyde) causes variation in droplet growth rate based on the composition of the surrounding droplets. These growth rate variations are partially transmitted after selective division of the largest droplets by shearing, which converts growth-rate differences into differences in droplet frequency. This shows how a combination of properties of living systems (growth, division, variation, competition, rudimentary heredity and selection) can arise from simple physical-chemical processes and may have paved the way for the emergence of evolution by natural selection.
Identifiants
pubmed: 37550391
doi: 10.1038/s41557-023-01276-0
pii: 10.1038/s41557-023-01276-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : EC | EC Seventh Framework Programm | FP7 Ideas: European Research Council (FP7-IDEAS-ERC - Specific Programme: 'Ideas ' Implementing the Seventh Framework Programme of the European Community for Research, Technological Development and Demonstration Activities (2007 to 2013))
ID : 294332
Organisme : EC | EC Seventh Framework Programm | FP7 Ideas: European Research Council (FP7-IDEAS-ERC - Specific Programme: 'Ideas ' Implementing the Seventh Framework Programme of the European Community for Research, Technological Development and Demonstration Activities (2007 to 2013))
ID : 294332
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-EQPX-34
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-EQPX-09
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-19-CE06-0010-01
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-EQPX-09
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-19-CE06-0010-01
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-10-EQPX-09
Organisme : Agence Nationale de la Recherche (French National Research Agency)
ID : ANR-19-CE06-0010-01
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Szathmáry, E. & Demeter, L. Group selection of early replicators and the origin of life. J. Theor. Biol. 128, 463–486 (1987).
pubmed: 2451771
doi: 10.1016/S0022-5193(87)80191-1
Matsumura, S. et al. Transient compartmentalization of RNA replicators prevents extinction due to parasites. Science 354, 1293–1296 (2016).
pubmed: 27940874
doi: 10.1126/science.aag1582
Bansho, Y., Furubayashi, T., Ichihashi, N. & Yomo, T. Host–parasite oscillation dynamics and evolution in a compartmentalized RNA replication system. Proc. Natl Acad. Sci. USA 113, 4045–4050 (2016).
pubmed: 27035976
pmcid: 4839452
doi: 10.1073/pnas.1524404113
Blokhuis, A., Lacoste, D., Nghe, P. & Peliti, L. Selection dynamics in transient compartmentalization. Phys. Rev. Lett. 120, 158101 (2018).
pubmed: 29756893
doi: 10.1103/PhysRevLett.120.158101
Blokhuis, A., Nghe, P., Peliti, L. & Lacoste, D. The generality of transient compartmentalization and its associated error thresholds. J. Theor. Biol. 487, 110110 (2020).
pubmed: 31837985
doi: 10.1016/j.jtbi.2019.110110
Vasas, V., Fernando, C., Santos, M., Kauffman, S. & Szathmáry, E. Evolution before genes. Biol. Direct 7, 1 (2012).
pubmed: 22221860
pmcid: 3284417
doi: 10.1186/1745-6150-7-1
Attwater, J., Raguram, A., Morgunov, A. S., Gianni, E. & Holliger, P. Ribozyme-catalysed RNA synthesis using triplet building blocks. eLife 7, e35255 (2018).
pubmed: 29759114
pmcid: 6003772
doi: 10.7554/eLife.35255
Horning, D. P. & Joyce, G. F. Amplification of RNA by an RNA polymerase ribozyme. Proc. Natl Acad. Sci. USA 113, 9786–9791 (2016).
pubmed: 27528667
pmcid: 5024611
doi: 10.1073/pnas.1610103113
Johnston, W. K., Unrau, P. J., Lawrence, M. S., Glasner, M. E. & Bartel, D. P. RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292, 1319–1325 (2001).
pubmed: 11358999
doi: 10.1126/science.1060786
Wochner, A., Attwater, J., Coulson, A. & Holliger, P. Ribozyme-catalyzed transcription of an active ribozyme. Science 332, 209–212 (2011).
pubmed: 21474753
doi: 10.1126/science.1200752
Joyce, G. F. & Szostak, J. W. Protocells and RNA self-replication. Cold Spring Harb. Perspect. Biol. 10, a034801–a034822 (2018).
pubmed: 30181195
pmcid: 6120706
doi: 10.1101/cshperspect.a034801
Walde, P., Wick, R., Fresta, M., Mangone, A. & Luisi, P. L. Autopoietic self-reproduction of fatty acid vesicles. J. Am. Chem. Soc. 116, 11649–11654 (1994).
doi: 10.1021/ja00105a004
Engwerda, A. H. J. et al. Coupled metabolic cycles allow out‐of‐equilibrium autopoietic vesicle replication. Angew. Chem. Int. Ed. 59, 20361–20366 (2020).
doi: 10.1002/anie.202007302
Kurihara, K. et al. Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat. Chem. 3, 775–781 (2011).
pubmed: 21941249
doi: 10.1038/nchem.1127
Bachmann, P. A., Luisi, P. L. & Lang, J. Autocatalytic self-replicating micelles as models for prebiotic structures. Nature 357, 57–59 (1992).
doi: 10.1038/357057a0
Colomer, I., Borissov, A. & Fletcher, S. P. Selection from a pool of self-assembling lipid replicators. Nat. Commun. 11, 176 (2020).
pubmed: 31924788
pmcid: 6954257
doi: 10.1038/s41467-019-13903-x
Matsuo, M. & Kurihara, K. Proliferating coacervate droplets as the missing link between chemistry and biology in the origins of life. Nat. Commun. 12, 5487 (2021).
pubmed: 34561428
pmcid: 8463549
doi: 10.1038/s41467-021-25530-6
Matsuo, M. et al. A sustainable self-reproducing liposome consisting of a synthetic phospholipid. Chem. Phys. Lipids 222, 1–7 (2019).
pubmed: 31002782
doi: 10.1016/j.chemphyslip.2019.04.007
Taylor, J. W., Eghtesadi, S. A., Points, L. J., Liu, T. & Cronin, L. Autonomous model protocell division driven by molecular replication. Nat. Commun. 8, 237 (2017).
pubmed: 28798300
pmcid: 5552811
doi: 10.1038/s41467-017-00177-4
Gánti, T. Organization of chemical reactions into dividing and metabolizing units: the chemotons. Biosystems 7, 15–21 (1975).
pubmed: 1156666
doi: 10.1016/0303-2647(75)90038-6
Boitard, L. et al. Monitoring single-cell bioenergetics via the coarsening of emulsion droplets. Proc. Natl Acad. Sci. USA 109, 7181–7186 (2012).
pubmed: 22538813
pmcid: 3358915
doi: 10.1073/pnas.1200894109
Butlerow, A. Formation synthétique d’une substance sucrée. C. R. Acad. Sci. 53, 145–147 (1861).
Breslow, R. On the mechanism of the formose reaction. Tetrahedron Lett. 21, 22–26 (1959).
doi: 10.1016/S0040-4039(01)99487-0
Appayee, C. & Breslow, R. Deuterium studies reveal a new mechanism for the formose reaction involving hydride shifts. J. Am. Chem. Soc. 136, 3720–3723 (2014).
pubmed: 24575857
doi: 10.1021/ja410886c
Socha, R. F., Weiss, A. H. & Sakharov, M. M. Homogeneously catalyzed condensation of formaldehyde to carbohydrates: VII. An overall formose reaction model. J. Catal. 67, 207–217 (1981).
doi: 10.1016/0021-9517(81)90272-4
Gruner, P. et al. Controlling molecular transport in minimal emulsions. Nat. Commun. 7, 10392 (2016).
pubmed: 26797564
pmcid: 4735829
doi: 10.1038/ncomms10392
Holtze, C. et al. Biocompatible surfactants for water-in-fluorocarbon emulsions. Lab Chip 8, 1632–1639 (2008).
pubmed: 18813384
doi: 10.1039/b806706f
Leal-Calderon, F., Schitt, V. & Bibette, J. Emulsion Science. Basic Principles 2nd edn (Springer, 2007).
Ricardo, A. et al. 2-Hydroxymethylboronate as a reagent to detect carbohydrates: application to the analysis of the formose reaction. J. Org. Chem. 71, 9503–9505 (2006).
pubmed: 17137382
doi: 10.1021/jo061770h
Maenaka, H., Yamada, M., Yasuda, M. & Seki, M. Continuous and size-dependent sorting of emulsion droplets using hydrodynamics in pinched microchannels. Langmuir 24, 4405–4410 (2008).
pubmed: 18327961
doi: 10.1021/la703581j
Kimura, M. & Crow, J. F. An Introduction to Population Genetics Theory (Blackburn Press, 1970).
Link, D. R., Anna, S. L., Weitz, D. A. & Stone, H. A. Geometrically mediated breakup of drops in microfluidic devices. Phys. Rev. Lett. 92, 054503 (2004).
pubmed: 14995311
doi: 10.1103/PhysRevLett.92.054503
Liao, Y. & Lucas, D. A literature review of theoretical models for drop and bubble breakup in turbulent dispersions. Chem. Eng. Sci. 64, 3389–3406 (2009).
doi: 10.1016/j.ces.2009.04.026
Benner, S. A. Paradoxes in the origin of life. Origins of life and evolution of the biosphere. J. Int. Soc. Stud. Orig. Life 44, 339–343 (2015).
Weiss, A. H., Seleznev, V. A. & Partridge, R. in Catalysis in Organic Synthesis (ed. Smith, G. V.) 153–164 (Academic, 1977).
Robinson, W. E., Daines, E., van Duppen, P., de Jong, T. & Huck, W. T. S. Environmental conditions drive self-organization of reaction pathways in a prebiotic reaction network. Nat. Chem. 14, 623–631 (2022).
pubmed: 35668214
doi: 10.1038/s41557-022-00956-7
Colón‐Santos, S., Cooper, G. J. T. & Cronin, L. Taming the combinatorial explosion of the formose reaction via recursion within mineral environments. ChemSystemsChem 1, e190001 (2019).
doi: 10.1002/syst.201900014
Gánti, T. The Principles of Life (Oxford Univ. Press, 2003).
Gánti, T. The Principles of Life (in Hungarian) (Gondolat, 1971).
Szathmáry, E. Life: in search of the simplest cell. Nature 433, 469–470 (2005).
pubmed: 15690023
doi: 10.1038/433469a
Gánti, T. The Principles of Life (in Hungarian) 2nd edn (Gondolat, 1978).
Gánti, T. Chemoton Theory. Vol. 2. Theory of Living Systems (Kluwer, 2003).
Gánti, T. Chemoton Theory. Vol. 1: Theoretical Foundations of Fluid Machineries (Kluwer, 2003).
Mavelli, F. & Ruiz-Mirazo, K. Stochastic simulations of minimal self-reproducing cellular systems. Phil. Trans. R. Soc. B 362, 1789–1802 (2007).
pubmed: 17510021
pmcid: 2515193
doi: 10.1098/rstb.2007.2071
Chen, I. A., Roberts, R. W. & Szostak, J. W. The emergence of competition between model protocells. Science 305, 1474–1476 (2004).
pubmed: 15353806
pmcid: 4484590
doi: 10.1126/science.1100757
Cheng, Z. & Luisi, P. L. Coexistence and mutual competition of vesicles with different size distributions. J. Phys. Chem. B 107, 10940–10945 (2003).
doi: 10.1021/jp034456p
Matsuo, M. et al. Environment-sensitive intelligent self-reproducing artificial cell with a modification-active lipo-deoxyribozyme. Micromachines (Basel) 11, 606 (2020).
pubmed: 32580457
pmcid: 7344958
doi: 10.3390/mi11060606
Qiao, Y., Li, M., Booth, R. & Mann, S. Predatory behaviour in synthetic protocell communities. Nat. Chem. 9, 110–119 (2017).
pubmed: 28282044
doi: 10.1038/nchem.2617
Mason, T. G. & Bibette, J. Shear rupturing of droplets in complex fluids. Langmuir 13, 4600–4613 (1997).
doi: 10.1021/la9700580
Adamala, K. & Szostak, J. W. Competition between model protocells driven by an encapsulated catalyst. Nat. Chem. 5, 495–501 (2013).
pubmed: 23695631
pmcid: 4041014
doi: 10.1038/nchem.1650
Stano, P. & Luisi, P. L. Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem. Commun. 46, 3639–3653 (2010).
doi: 10.1039/b913997d
Kurihara, K. et al. A recursive vesicle-based model protocell with a primitive model cell cycle. Nat. Commun. 6, 8352 (2015).
pubmed: 26418735
doi: 10.1038/ncomms9352
Segré, D., Ben-Eli, D. & Lancet, D. Compositional genomes: prebiotic information transfer in mutually catalytic noncovalent assemblies. Proc. Natl Acad. Sci. USA 97, 4112–4117 (2000).
pubmed: 10760281
pmcid: 18166
doi: 10.1073/pnas.97.8.4112
Eigen, M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58, 465–523 (1971).
pubmed: 4942363
doi: 10.1007/BF00623322
Vasas, V., Szathmary, E. & Santos, M. Lack of evolvability in self-sustaining autocatalytic networks constraints metabolism-first scenarios for the origin of life. Proc. Natl Acad. Sci. USA 107, 1470–1475 (2010).
pubmed: 20080693
pmcid: 2824406
doi: 10.1073/pnas.0912628107
Sommer, R. J. Phenotypic plasticity: from theory and genetics to current and future challenges. Genetics 215, 1–13 (2020).
pubmed: 32371438
pmcid: 7198268
doi: 10.1534/genetics.120.303163
Angeli, D., Ferrell, J. E. & Sontag, E. D. Detection of multistability, bifurcations and hysteresis in a large class of biological positive-feedback systems. Proc. Natl Acad. Sci. USA 101, 1822–1827 (2004).
pubmed: 14766974
pmcid: 357011
doi: 10.1073/pnas.0308265100
Blokhuis, A., Lacoste, D. & Nghe, P. Universal motifs and the diversity of autocatalytic systems. Proc. Natl Acad. Sci. USA 117, 25230–25236 (2020).
pubmed: 32989134
pmcid: 7568248
doi: 10.1073/pnas.2013527117
Duffy, D. C., McDonald, J. C., Schueller, O. J. & Whitesides, G. M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70, 4974–4984 (1998).
pubmed: 21644679
doi: 10.1021/ac980656z
Mazutis, L. et al. Single-cell analysis and sorting using droplet-based microfluidics. Nat. Protoc. 8, 870–891 (2013).
pubmed: 23558786
pmcid: 4128248
doi: 10.1038/nprot.2013.046
Eyer, K. et al. Single-cell deep phenotyping of IgG-secreting cells for high-resolution immune monitoring. Nat. Biotechnol. 35, 977–982 (2017).
pubmed: 28892076
doi: 10.1038/nbt.3964
Anna, S. L., Bontoux, N. & Stone, H. A. Formation of dispersions using ‘flow focusing’ in microchannels. Appl. Phys. Lett. 82, 364–366 (2003).
doi: 10.1063/1.1537519
Nash, T. The colorimetric estimation of formaldehyde by means of the Hantzsch reaction. Biochem. J. 55, 416–421 (1953).
pubmed: 13105648
pmcid: 1269292
doi: 10.1042/bj0550416
Nghe, P., Lu, H. & Karuppusamy, J. Image analysis code for droplets containing formose reaction (Zenodo, 2022); https://zenodo.org/record/7130398
Blokhuis, A. & Nghe, P. Formose reaction droplet simulation code (Zenodo, 2022); https://zenodo.org/record/7140351