Abstract
In the past years, artificial cellular models for origins-of-life research and synthetic biology have been extensively studied. At this aim, solute-filled lipid vesicles (liposomes) are widely used. Several evidences have been collected about the capture of water-soluble chemicals, the mechanism of vesicle self-reproduction, and the course of (bio)chemical reactions in the vesicle lumen. Among the several fascinating questions which emerged from these studies, here we focus on a peculiar feature, namely, the fact that a spontaneous heterogeneity of vesicle structure often emerges. In other words, vesicle populations created in the laboratory by classical batch methods include very ‘diverse’ vesicles with respect to size, morphology, and – importantly – solute content. The consequences of this between-vesicle diversity are shortly discussed.
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Notes
- 1.
Ideally, one would like to have a single lipid monolayer deposited over a large surface so that all parts of the film would experience the same conditions. This corresponds, in most cases, to work well below the \(\mu \)M lipid concentration range, with consequent vesicle losses and other impractical complications. Thus, in the most common experimental conditions the film is rarely so perfect and different regions of the film will experience different micro-environments. Actually, realistic laboratory conditions might affect the measured heterogeneity of vesicle formation paths.
- 2.
Note that this loss does not refer to the volume loss which follows from the vesicle size reduction, but it is an authentic concentration reduction due to the reduction of the average number per unit of volume.
References
Altamura, E., Carrara, P., D’Angelo, F., Mavelli, F., Stano, P.: Extrinsic stochastic factors (solute partition) in gene expression inside lipid vesicles and lipid-stabilized water-in-oil droplets. Synth. Biol. (OUP) p. (2018, in press)
Bangham, A.D., Horne, R.W.: Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J. Mol. Biol. 8, 660–668 (1964)
Calviello, L., Stano, P., Mavelli, F., Luisi, P.L., Marangoni, R.: Quasi-cellular systems: stochastic simulation analysis at nanoscale range. BMC Bioinf. 14, S7 (2013). https://doi.org/10.1186/1471-2105-14-S7-S7
Carrara, P., Stano, P., Luisi, P.L.: Giant vesicles “colonies”: a model for primitive cell communities. Chembiochem Eur. J. Chem. Biol. 13(10), 1497–1502 (2012). https://doi.org/10.1002/cbic.201200133
D’Aguanno, E., Altamura, E., Mavelli, F., Fahr, A., Stano, P., Luisi, P.L.: Physical routes to primitive cells: an experimental model based on the spontaneous entrapment of enzymes inside micrometer-sized liposomes. Life (Basel, Switzerland) 5(1), 969–996 (2015). https://doi.org/10.3390/life5010969
Damiano, L., Canamero, L.: The frontier of synthetic knowledge: toward a constructivist science. World Futures 68(3), 171–177 (2012). https://doi.org/10.1080/02604027.2012.668409
Elani, Y.: Construction of membrane-bound artificial cells using microfluidics: a new frontier in bottom-up synthetic biology. Biochem. Soc. Trans. 44(3), 723–730 (2016). https://doi.org/10.1042/BST20160052
Exterkate, M., Caforio, A., Stuart, M.C.A., Driessen, A.J.M.: Growing membranes in vitro by continuous phospholipid biosynthesis from free fatty acids. ACS Synth. Biol. 7(1), 153–165 (2018). https://doi.org/10.1021/acssynbio.7b00265
Fanti, A., Gammuto, L., Mavelli, F., Stano, P., Marangoni, R.: Do protocells preferentially retain macromolecular solutes upon division/fragmentation? A study based on the extrusion of POPC giant vesicles. Integr. Biol. (Camb) 10(1), 6–17 (2018). https://doi.org/10.1039/c7ib00138j
Fox, S.V.: Self-assembly of the protocell from a self-ordered polymer. J. Sci. Ind. Res. 27, 267–274 (1968)
Gebicki, J.M., Hicks, M.: Ufasomes are stable particles surrounded by unsaturated fatty acid membranes. Nature 243(5404), 232–234 (1973)
Hadorn, M., Boenzli, E., Sørensen, K.T., De Lucrezia, D., Hanczyc, M.M., Yomo, T.: Defined DNA-mediated assemblies of gene-expressing giant unilamellar vesicles. Langmuir 29(49), 15309–15319 (2013). https://doi.org/10.1021/la402621r
Hanczyc, M.M.: The early history of protocells - the search for the recipe of life. In: Rasmussen, S., et al. (eds.) Protocells Bridging Nonliving and Living Matter. MIT Press, Cambridge (2009)
Hanczyc, M.M., Fujikawa, S.M., Szostak, J.W.: Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302(5645), 618–622 (2003). https://doi.org/10.1126/science.1089904
Hargreaves, W.R., Deamer, D.W.: Liposomes from ionic, single-chain amphiphiles. Biochemistry 17(18), 3759–3768 (1978)
Hosoda, K., Sunami, T., Kazuta, Y., Matsuura, T., Suzuki, H., Yomo, T.: Quantitative study of the structure of multilamellar giant liposomes as a container of protein synthesis reaction. Langmuir 24(23), 13540–13548 (2008). https://doi.org/10.1021/la802432f
Kaneko, K.: Life: An Introduction to Complex Systems Biology. UCS. Springer, Heidelberg (2006). https://doi.org/10.1007/978-3-540-32667-0
Kita, H., et al.: Replication of genetic information with self-encoded replicase in liposomes. ChemBioChem. 9(15), 2403–2410 (2008). https://doi.org/10.1002/cbic.200800360
Kuruma, Y., Stano, P., Ueda, T., Luisi, P.L.: A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim. Biophys. Acta 1788(2), 567–574 (2009). https://doi.org/10.1016/j.bbamem.2008.10.017
Lazzerini-Ospri, L., Stano, P., Luisi, P., Marangoni, R.: Characterization of the emergent properties of a synthetic quasi-cellular system. BMC Bioinform. 13(Suppl 4), S9 (2012). https://doi.org/10.1186/1471-2105-13-S4-S9
Luisi, P.L.: Autopoiesis: a review and a reappraisal. Naturwissenschaften 90(2), 49–59 (2003). https://doi.org/10.1007/s00114-002-0389-9
Luisi, P.L., Allegretti, M., Pereira de Souza, T., Steiniger, F., Fahr, A., Stano, P.: Spontaneous protein crowding in liposomes: a new vista for the origin of cellular metabolism. ChemBioChem 11(14), 1989–1992 (2010). https://doi.org/10.1002/cbic.201000381
Maturana, H.R., Varela, F.J.: Autopoiesis and Cognition: The Realization of the Living. D. Reidel Publishing Company, 1st edn. (1980)
Mavelli, F.: Stochastic simulations of minimal cells: the Ribocell model. BMC Bioinform. 13(Suppl 4), S10 (2012). https://doi.org/10.1186/1471-2105-13-S4-S10
Mavelli, F., Stano, P.: Experiments on and numerical modeling of the capture and concentration of transcription-translation machinery inside vesicles. Artif. Life 21(4), 445–463 (2015)
Nakano, T., Eckford, A.W., Haraguchi, T.: Molecular Communications. Cambridge University Press, Cambridge UK (2013)
Oparin, A.I.: The pathways of the primary development of metabolism and artificial modeling of this development in coacervate drops. In: The Origins of Prebiological Systems and of their Molecular Matrices, pp. 331–345. S. W. Fox, New York, Academic Press edn. (1965)
Paradisi, P., Allegrini, P., Chiarugi, D.: A renewal model for the emergence of anomalous solute crowding in liposomes. BMC Syst. Biol. 9(Suppl 3), S7 (2015). https://doi.org/10.1186/1752-0509-9-S3-S7
Rampioni, G., et al.: Synthetic cells produce a quorum sensing chemical signal perceived by Pseudomonas aeruginosa. Chem. Commun. 54, 2090–2093 (2018). https://doi.org/10.1039/C7CC09678J
Schmidli, P., Schurtenberger, P., Luisi, P.: Liposome-mediated enzymatic-synthesis of phosphatidylcholine as an approach to self-replicating liposomes. J. Am. Chem. Soc. 113(21), 8127–8130 (1991). https://doi.org/10.1021/ja00021a043
Pereira de Souza, T., Stano, P., Luisi, P.L.: The minimal size of liposome-based model cells brings about a remarkably enhanced entrapment and protein synthesis. Chembiochem 10(6), 1056–1063 (2009). https://doi.org/10.1002/cbic.200800810
de Souza, T.P., Fahr, A., Luisi, P.L., Stano, P.: Spontaneous encapsulation and concentration of biological macromolecules in liposomes: an intriguing phenomenon and its relevance in origins of life. J. Mol. Evol. 79(5–6), 179–192 (2014). https://doi.org/10.1007/s00239-014-9655-7
Souza, T.P.D., et al.: Vesicle aggregates as a model for primitive cellular assemblies. Phys. Chem. Chem. Phys. 19(30), 20082–20092 (2017). https://doi.org/10.1039/C7CP03751A
Stano, P., Wehrli, E., Luisi, P.L.: Insights into the self-reproduction of oleate vesicles. J. Phys. Condens. Matter 18(33), S2231 (2006). https://doi.org/10.1088/0953-8984/18/33/S37
Stano, P., Carrara, P., Kuruma, Y., de Souza, T.P., Luisi, P.L.: Compartmentalized reactions as a case of soft-matter biotechnology: synthesis of proteins and nucleic acids inside lipid vesicles. J. Mater. Chem. 21(47), 18887–18902 (2011). https://doi.org/10.1039/c1jm12298c
Stano, P., D’Aguanno, E., Bolz, J., Fahr, A., Luisi, P.L.: A remarkable self-organization process as the origin of primitive functional cells. Angew. Chemie-Int. Ed. 52(50), 13397–13400 (2013). https://doi.org/10.1002/anie.201306613
Stano, P., Luisi, P.: Theory and construction of semi-synthetic minimal cells. In: Nesbeth, D.N. (ed.) Synthetic Biology Handbook, pp. 209–258. CRC Press, London (2016)
Stano, P., Mavelli, F.: Protocells models in origin of life and synthetic biology. Life 5(4), 1700–1702 (2015). https://doi.org/10.3390/life5041700
Stano, P., et al.: Recent biophysical issues about the preparation of solute-filled lipid vesicles. Mech. Adv. Mater. Struct. 22(9), 748–759 (2015). https://doi.org/10.1080/15376494.2013.857743
van Swaay, D., deMello, A.: Microfluidic methods for forming liposomes. Lab. Chip. 13(5), 752–767 (2013). https://doi.org/10.1039/c2lc41121k
Walde, P., Wick, R., Fresta, M., Mangone, A., Luisi, P.: Autopoietic self-reproduction of fatty-acid vesicles. J. Am. Chem. Soc. 116(26), 11649–11654 (1994). https://doi.org/10.1039/c2lc41121k
Weiss, M., et al.: Sequential bottom-up assembly of mechanically stabilized synthetic cells by microfluidics. Nat. Mater. 17(1), 89–96 (2018). https://doi.org/10.1038/nmat5005
Zepik, H.H., Blochliger, E., Luisi, P.L.: A chemical model of homeostasis. Angew. Chem.-Int. Edit. 40(1), 199–202 (2001)
Zhu, T.F., Szostak, J.W.: Coupled growth and division of model protocell membranes. J. Am. Chem. Soc. 131(15), 5705–5713 (2009). https://doi.org/10.1021/ja900919c
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Collaboration among the authors has been fostered by the European COST Action CM1304 Emergence and Evolution of Complex Chemical Systems.
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Stano, P., Marangoni, R., Mavelli, F. (2019). Experimental Evidences Suggest High Between-Vesicle Diversity of Artificial Vesicle Populations: Results, Models and Implications. In: Bartoletti, M., et al. Computational Intelligence Methods for Bioinformatics and Biostatistics. CIBB 2017. Lecture Notes in Computer Science(), vol 10834. Springer, Cham. https://doi.org/10.1007/978-3-030-14160-8_17
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