Skip to main content

Minimal Cellular Models for Origins-of-Life Studies and Biotechnology

  • Chapter
  • First Online:
The Biophysics of Cell Membranes

Part of the book series: Springer Series in Biophysics ((BIOPHYSICS,volume 19))

Abstract

Minimal cellular models can be defined as those vesicle-based cell-like constructs that are assembled with the aim of (1) clarifying/understanding unknown aspects in origins-of-life research and hypotheses testing, (2) studying reconstituted biochemical pathways in a simplified system, (3) being exploited for potential biotechnological applications, and (4) developing novel concepts/technologies. These ‘synthetic cells’ are created by the bottom-up approach and within the synthetic/constructive paradigm. Here we shortly review the main ideas behind such novel usage of vesicles, and comment the experimental data collected in the past decades. An intriguing picture emerges, where technical progresses owing to the convergence of liposome, cell-free (and microfluidic) technologies lead to a fecund research area of great potential, which blends fundamental scientific question with the most modern and challenging facets of synthetic biology.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Haldane JBS (1929) The origin of life. Ration Annu 148:3–10

    Google Scholar 

  2. Oparin AI (1953) The origin of life, 2nd edn. (Tras: Morgulis S). Dover Publications, New York

    Google Scholar 

  3. Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117(3046):528–529

    Article  CAS  PubMed  Google Scholar 

  4. Ruiz-Mirazo K, Briones C, de la Escosura A (2014) Prebiotic systems chemistry: new perspectives for the origins of life. Chem Rev 114(1):285–366

    Article  CAS  PubMed  Google Scholar 

  5. Hanczyc MM (2009) The early history of protocells – the search for the recipe of life. In: Rasmussen S, Bedau MA, Chen L, Deamer D, Krakauer DC, Packard NH, Stadler PF (eds) Protocells: bridging nonliving and living matter. MIT Press, Cambridge, pp 3–18

    Google Scholar 

  6. Jia TZ, Hentrich C, Szostak JW (2014) Rapid RNA exchange in aqueous two-phase system and coacervate droplets. Orig Life Evol Biosph 44:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. van Swaay D, Dora Tang T-Y, Mann S, de Mello A (2015) Microfluidic formation of membrane-free aqueous coacervate droplets in water. Angew Chem Int Ed Engl 54(29):8398–8401

    Article  PubMed  CAS  Google Scholar 

  8. Dora Tang T-Y, van Swaay D, deMello A, Ross Anderson JL, Mann S (2015) In vitro gene expression within membrane-free coacervate protocells. Chem Commun (Camb) 51(57):11429–11432

    Article  CAS  Google Scholar 

  9. Bangham AD, Horne RW (1964) Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J Mol Biol 8:660–668

    Article  CAS  PubMed  Google Scholar 

  10. Bangham AD, Standish MM, Watkins JC (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J Mol Biol 13(1):238–252

    Article  CAS  PubMed  Google Scholar 

  11. Luisi PL, Ferri F, Stano P (2006) Approaches to semi-synthetic minimal cells: a review. Naturwissenschaften 93(1):1–13

    Article  CAS  PubMed  Google Scholar 

  12. Mansy SS, Szostak JW (2009) Reconstructing the emergence of cellular life through the synthesis of model protocells. Cold Spring Harb Symp Quant Biol 74:47–54

    Article  CAS  PubMed  Google Scholar 

  13. Ichihashi N, Yomo T (2016) Constructive approaches for understanding the origin of self-replication and evolution. Life (Basel) 6(3)

    Google Scholar 

  14. de Lorenzo V, Danchin A (2008) Synthetic biology: discovering new worlds and new words. EMBO Rep 9(9):822–827

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Pohorille A, Deamer D (2002) Artificial cells: prospects for biotechnology. Trends Biotechnol 20(3):123–128

    Article  CAS  PubMed  Google Scholar 

  16. Noireaux V, Maeda YT, Libchaber A (2011) Development of an artificial cell, from self-organization to computation and self-reproduction. PNAS 108(9):3473–3480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Stano P (2011) Minimal cells: relevance and interplay of physical and biochemical factors. Biotechnol J 6(7):850–859

    Article  CAS  PubMed  Google Scholar 

  18. Stano P, Rampioni G, Carrara P, Damiano L, Leoni L, Luisi PL (2012) Semi-synthetic minimal cells as a tool for biochemical ICT. BioSystems 109(1):24–34

    Article  CAS  PubMed  Google Scholar 

  19. Ichihashi N, Aita T, Motooka D, Nakamura S, Yomo T (2015) Periodic pattern of genetic and fitness diversity during evolution of an artificial cell-like system. Mol Biol Evol 32(12):3205–3214

    CAS  PubMed  Google Scholar 

  20. Xu C, Hu S, Chen X (2016) Artificial cells: from basic science to applications. Mater Today 19(9):516–532

    Article  CAS  Google Scholar 

  21. Gebicki Jm, Hicks M (1973) Ufasomes are stable particles surrounded by unsaturated fatty-acid membranes. Nature 243(5404):232–234

    Article  Google Scholar 

  22. Ourisson G, Nakatani Y (1994) The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol. Chem Biol 1(1):11–23

    Article  CAS  PubMed  Google Scholar 

  23. Pozzi G, Birault V, Werner B, Dannenmuller O, Nakatani Y, Ourisson G, Terakawa S (1996) Single-chain polyprenyl phosphates form primitive membranes. Angew Chem Int Ed Engl 35(2):177–180

    Article  CAS  Google Scholar 

  24. Streiff S, Ribeiro N, Wu Z, Gumienna-Kontecka E, Elhabiri M, Albrecht-Gary AM, Ourisson G, Nakatani Y (2007) “Primitive” membrane from polyprenyl phosphates and polyprenyl alcohols. Chem Biol 14(3):313–319

    Article  CAS  PubMed  Google Scholar 

  25. Nakatani Y, Ribeiro N, Streiff S, Gotoh M, Pozzi G, Dsaubry L, Milon A (2014) Search for the most primitive membranes and their reinforcers: a review of the polyprenyl phosphates theory. Orig Life Evol Biosph 44(3):197–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Discher BM, Won YY, Ege DS, Lee JCM, Bates FS, Discher DE, Hammer DA (1999) Polymersomes: Tough vesicles made from diblock copolymers. Science 284(5417):1143–1146

    Article  CAS  PubMed  Google Scholar 

  27. Choi H-J, Montemagno CD (2005) Artificial organelle: ATP synthesis from cellular mimetic polymersomes. Nano Lett 5(12):2538–2542

    Article  CAS  PubMed  Google Scholar 

  28. Chandrawati R, Caruso F (2012) Biomimetic liposome- and polymersome-based multicompartmentalized assemblies. Langmuir 28(39):13798–13807

    Article  CAS  PubMed  Google Scholar 

  29. Martino C, Shin-Hyun Kim, Horsfall L, Abbaspourrad A, Rosser SJ, Cooper J, Weitz DA (2012) Protein expression, aggregation, and triggered release from polymersomes as artificial cell-like structures. Angew Chem-Int Edit 51(26):6416–6420

    Article  CAS  Google Scholar 

  30. Walde P, Cosentino K, Engel H, Stano P (2010) Giant vesicles: preparations and applications. Chembiochem 11(7):848–865

    Article  CAS  PubMed  Google Scholar 

  31. Walde P (2004) Preparation of vesicles (liposomes). In: Encyclopedia of nanoscience and nanotechnology, vol 9. H. S. Nalwa, American Scientific Publishers, pp 43–79

    Google Scholar 

  32. Walde P (2006) Surfactant assemblies and their various possible roles for the origin(s) of life. Orig Life Evol Biosph 36(2):109–150

    Article  CAS  PubMed  Google Scholar 

  33. Namani T, Walde P (2005) From decanoate micelles to decanoic acid/dodecylbenzenesulfonate vesicles. Langmuir 21(14):6210–6219

    Article  CAS  PubMed  Google Scholar 

  34. Walde P, Wick R, Fresta M, Mangone A, Luisi PL (1994) Autopoietic self-reproduction of fatty-acid vesicles. J Am Chem Soc 116(26):11649–11654

    Article  CAS  Google Scholar 

  35. Walde P, Goto A, Monnard Pa, Wessicken M, Luisi Pl (1994) Oparins reactions revisited – enzymatic-synthesis of poly (adenylic Acid). J Am Chem Soc 116(17):7541–7547

    Article  CAS  Google Scholar 

  36. Blöchliger E, Blocher M, Walde P, Luisi PL (1998) Matrix effect in the size distribution of fatty acid vesicles. J Phys Chem B 102(50):10383–10390

    Article  Google Scholar 

  37. Lonchin S, Luisi PL, Walde P, Robinson BH (1999) A matrix effect in mixed phospholipid/fatty acid vesicle formation. J Phys Chem B 103(49):10910–10916

    Article  CAS  Google Scholar 

  38. Berclaz N, Blöchliger E, Müller M, Luisi PL (2001) Matrix effect of vesicle formation as investigated by cryotransmission electron microscopy. J Phys Chem B 105(5):1065–1071

    Article  CAS  Google Scholar 

  39. Rasi S, Mavelli F, Luisi PL (2003) Cooperative micelle binding and matrix effect in oleate vesicle formation. J Phys Chem B 107(50):14068–14076

    Article  CAS  Google Scholar 

  40. Chen IA, Roberts RW, Szostak JW (2004) The emergence of competition between model protocells. Science 305(5689):1474–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chen IA, Szostak JW (2004) A kinetic study of the growth of fatty acid vesicles. Biophys J 87(2):988–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhu TF, Szostak JW (2009) Coupled growth and division of model protocell membranes. J Am Chem Soc 131(15):5705–5713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Fujikawa SM, Chen IA, Szostak JW (2005) Shrink-wrap vesicles. Langmuir 21(26):12124–12129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mansy SS, Schrum JP, Krishnamurthy M, Tobé S, Treco DA, Szostak JW (2008) Template-directed synthesis of a genetic polymer in a model protocell. Nature 454(7200):122–U10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mansy SS, Szostak JW (2008) Thermostability of model protocell membranes. Proc Natl Acad Sci USA 105(36):13351–13355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Engelhart AE, Adamala KP, Szostak JW (2016) A simple physical mechanism enables homeostasis in primitive cells. Nat Chem 8(5):448–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rendón A, Carton DG, Sot J, García-Pacios M, Montes L-R, Valle M, Arrondo J-LR, Goñi FM, Ruiz-Mirazo K (2012) Model systems of precursor cellular membranes: long-chain alcohols stabilize spontaneously formed oleic acid vesicles. Biophys J 102(2): 278–286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Birault V, Pozzi G, Plobeck N, Eifler S, Schmutz M, Palanché T, Raya J, Brisson A, Nakatani Y, Ourisson G (1996) Di(polyprenyl) phosphates as models for primitive membrane constituents: synthesis and phase properties. Chem Eur J 2(7):789–799

    Article  CAS  Google Scholar 

  49. Gotoh M, Miki A, Nagano H, Ribeiro N, Elhabiri M, Gumienna-Kontecka E, Albrecht-Gary A-M, Schmutz M, Ourisson G, Nakatani Y (2006) Membrane properties of branched polyprenyl phosphates, postulated as primitive membrane constituents. Chem Biodivers 3(4):434–455

    Article  CAS  PubMed  Google Scholar 

  50. Monnard PA, Deamer DW (2002) Membrane self-assembly processes: steps toward the first cellular life. Anat Rec 268(3):196–207

    Article  CAS  PubMed  Google Scholar 

  51. Namani T, Deamer DW (2008) Stability of model membranes in extreme environments. Orig Life Evol Biosph, 38(4):329–341

    Article  CAS  PubMed  Google Scholar 

  52. Monnard P-A, Apel CL, Kanavarioti A, Deamer DW (2002) Influence of ionic inorganic solutes on self-assembly and polymerization processes related to early forms of life: implications for a prebiotic aqueous medium. Astrobiology 2(2):139–152

    Article  CAS  PubMed  Google Scholar 

  53. Maurer SE, Deamer DW, Boncella JM, Monnard P-A (2009) Chemical evolution of amphiphiles: glycerol monoacyl derivatives stabilize plausible prebiotic membranes. Astrobiology 9(10):979–987

    Article  CAS  PubMed  Google Scholar 

  54. Adamala K, Szostak JW (2013) Nonenzymatic template-directed RNA synthesis inside model protocells. Science 342(6162):1098–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Israelachvili JN, John Mitchell D, Ninham BW (1976) Theory of self-assembly of hydrocarbon amphiphiles into micelles and bilayers. J Chem Soc Faraday Trans 2 72(0): 1525–1568

    Google Scholar 

  56. (1999) Steering Group for the workshop on size limits of very small microorganisms National Research Council. In: Knoll A, Osborn MJ, Baross J, Berg HC, Pace NR, Sogin M (eds) Size limits of very small microorganisms: proceedings of a workshop. National Academic Press, Washington, DC

    Google Scholar 

  57. Pereira de Souza T, Stano P, Luisi PL (2009) The minimal size of liposome-based model cells brings about a remarkably enhanced entrapment and protein synthesis. Chembiochem 10(6):1056–1063

    Article  CAS  PubMed  Google Scholar 

  58. Akashi K, Miyata H, Itoh H, Kinosita K (1996) Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Biophys J 71(6):3242–3250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Carrara P, Stano P, Luisi PL (2012) Giant vesicles “colonies”: a model for primitive cell communities. Chembiochem 13(10):1497–1502

    Article  CAS  PubMed  Google Scholar 

  60. Pautot S, Frisken BJ, Weitz DA (2003) Production of unilamellar vesicles using an inverted emulsion. Langmuir 19(7):2870–2879

    Article  CAS  Google Scholar 

  61. Noireaux V, Libchaber A (2004) A vesicle bioreactor as a step toward an artificial cell assembly. Proc Natl Acad Sci USA 101(51):17669–17674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Pautot S, Frisken BJ, Weitz DA (2003) Engineering asymmetric vesicles. Proc Natl Acad Sci USA 100(19):10718–10721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Stano P, Wodlei F, Carrara P, Ristori S, Marchettini N, Rossi F (2014) Approaches to molecular communication between synthetic compartments based on encapsulated chemical oscillators. In: Pizzuti C, Spezzano G (eds) Advances in artificial life and evolutionary computation. WIVACE 2014. Volume 445 of communications in computer and information science. Springer, Cham

    Google Scholar 

  64. Sugiura S, Kuroiwa T, Kagota T, Nakajima M, Sato S, Mukataka S, Walde P, Ichikawa S (2008) Novel method for obtaining homogeneous giant vesicles from a monodisperse water-in-oil emulsion prepared with a microfluidic device. Langmuir 24(9):4581–4588

    Article  CAS  PubMed  Google Scholar 

  65. Matosevic S, Paegel BM (2011) Stepwise synthesis of giant unilamellar vesicles on a microfluidic assembly line. J Am Chem Soc 133(9):2798–2800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Hu PC, Li S, Malmstadt N (2011) Microfluidic fabrication of asymmetric giant lipid vesicles. ACS Appl Mater Interfaces 3(5):1434–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Nishimura K, Suzuki H, Toyota T, Yomo T (2012) Size control of giant unilamellar vesicles prepared from inverted emulsion droplets. J Colloid Interface Sci 376(1):119–125

    Article  CAS  PubMed  Google Scholar 

  68. Matosevic S (2012) Synthesizing artificial cells from giant unilamellar vesicles: state-of-the art in the development of microfluidic technology. Bioessays 34(11):992–1001

    Article  CAS  PubMed  Google Scholar 

  69. Shiomi H, Tsuda S, Suzuki H, Yomo T (2014) Liposome-based liquid handling platform featuring addition, mixing, and aliquoting of femtoliter volumes. PLoS ONE 9(7):e101820

    Article  PubMed  PubMed Central  Google Scholar 

  70. Karamdad K, Law RV, Seddon JM, Brooks NJ, Ces O (2015) Preparation and mechanical characterisation of giant unilamellar vesicles by a microfluidic method. Lab Chip 15(2): 557–562

    Article  CAS  PubMed  Google Scholar 

  71. Morita M, Onoe H, Yanagisawa M, Ito H, Ichikawa M, Fujiwara K, Saito H, Takinoue M (2015) Droplet-shooting and size-filtration (DSSF) method for synthesis of cell-sized liposomes with controlled lipid compositions. Chembiochem 16(14):2029–2035

    Article  CAS  PubMed  Google Scholar 

  72. Deamer DW, Prince RC, Crofts AR (1972) The response of fluorescent amines to pH gradients across liposome membranes. Biochim Biophys Acta 274(2):323–335

    Article  CAS  PubMed  Google Scholar 

  73. Haran G, Cohen R, Bar LK, Barenholz Y (1993) Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim Biophys Acta 1151(2):201–215

    Article  CAS  PubMed  Google Scholar 

  74. Cullis PR, Hope MJ, Bally MB, Madden TD, Mayer LD, Fenske DB (1997) Influence of pH gradients on the transbilayer transport of drugs, lipids, peptides and metal ions into large unilamellar vesicles. Biochim Biophys Acta 1331(2):187–211

    Article  CAS  PubMed  Google Scholar 

  75. Chakrabarti AC, Deamer DW (1992) Permeability of lipid bilayers to amino acids and phosphate. Biochim Biophys Acta 1111(2):171–177

    Article  CAS  PubMed  Google Scholar 

  76. Chakrabarti AC (1994) Permeability of membranes to amino acids and modified amino acids: mechanisms involved in translocation. Amino Acids 6:213–229

    Article  CAS  Google Scholar 

  77. Chakrabarti AC, Deamer DW (1994) Permeation of membranes by the neutral form of amino acids and peptides: relevance to the origin of peptide translocation. J Mol Evol 39(1):1–5

    Article  PubMed  Google Scholar 

  78. Monnard PA, Deamer DW (2001) Nutrient uptake by protocells: a liposome model system. Orig Life Evol Biosph 31(1-2):147–155

    Article  CAS  PubMed  Google Scholar 

  79. Batzri S, Korn ED (1973) Single bilayer liposomes prepared without sonication. Biochimica et Biophysica Acta (BBA) – Biomembranes 298(4):1015–1019

    Article  CAS  Google Scholar 

  80. Dominak LM, Keating CD (2007) Polymer encapsulation within giant lipid vesicles. Langmuir 23(13):7148–7154

    Article  CAS  PubMed  Google Scholar 

  81. Lohse B, Bolinger P-Y, Stamou D (2008) Encapsulation efficiency measured on single small unilamellar vesicles. J Am Chem Soc 130(44):14372–14373

    Article  CAS  PubMed  Google Scholar 

  82. Luisi PL, Allegretti M, de Souza TP, Steiniger F, Fahr A, Stano P (2010) Spontaneous protein crowding in liposomes: a new vista for the origin of cellular metabolism. ChemBioChem 11(14):1989–1992

    Article  CAS  PubMed  Google Scholar 

  83. Nishimura K, Hosoi T, Sunami T, Toyota T, Fujinami M, Oguma K, Matsuura T, Suzuki H, Yomo T (2009) Population analysis of structural properties of giant liposomes by flow cytometry. Langmuir 25(18):10439–10443

    Article  CAS  PubMed  Google Scholar 

  84. Sakakura T, Nishimura K, Suzuki H, Yomo T (2012) Statistical analysis of discrete encapsulation of nanomaterials in colloidal capsules. Anal Methods 4(6):1648–1655

    Article  CAS  Google Scholar 

  85. Stano P, de Souza TP, Carrara P, Altamura E, D’Aguanno E, Caputo M, Luisi PL, Mavelli F (2015) Recent biophysical issues about the preparation of solute-filled lipid vesicles. Mech Adv Mater Struct 22(9):748–759

    Article  Google Scholar 

  86. Cheng Z, Luisi PL (2003) Coexistence and mutual competition of vesicles with different size distributions. J Phys Chem B 107(39):10940–10945

    Article  CAS  Google Scholar 

  87. Adamala K, Szostak JW (2013) Competition between model protocells driven by an encapsulated catalyst. Nat Chem 5(6):495–501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Adamala KP, Engelhart AE, Szostak JW (2016) Collaboration between primitive cell membranes and soluble catalysts. Nat Commun 7:11041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Boukobza E, Sonnenfeld A, Haran G (2001) Immobilization in surface-tethered lipid vesicles as a new tool for single biomolecule spectroscopy. J Phys Chem B 105(48):12165–12170

    Article  CAS  Google Scholar 

  90. Pereira de Souza T, Fahr A, Luisi PL, Stano P (2014) Spontaneous encapsulation and concentration of biological macromolecules in liposomes: an intriguing phenomenon and its relevance in origins of life. J Mol Evol 1–14

    Google Scholar 

  91. de Souza TP, Steiniger F, Stano P, Fahr A, Luisi PL. Spontaneous crowding of ribosomes and proteins inside vesicles: a possible mechanism for the origin of cell metabolism. Chembiochem 12(15):2325–2330 (2011)

    Article  CAS  Google Scholar 

  92. Stano P, Erica D’Aguanno, Jürgen Bolz, Fahr A, Luisi PL (2013) A remarkable self-organization process as the origin of primitive functional cells. Angew Chem Int Ed Engl 52(50):13397–13400

    Article  CAS  PubMed  Google Scholar 

  93. Mavelli F, Stano P (2015) Experiments on and numerical modeling of the capture and concentration of transcription-translation machinery inside vesicles. Artif Life 21(4): 445–463

    Article  PubMed  Google Scholar 

  94. D’Aguanno E, Altamura E, Mavelli F, Fahr A, Stano P, Luisi PL (2015) Physical routes to primitive cells: an experimental model based on the spontaneous entrapment of enzymes inside micrometer-sized liposomes. Life 5(1):969–996

    Article  PubMed  PubMed Central  Google Scholar 

  95. van Hoof B, Markvoort AJ, van Santen RA, Peter Hilbers AJ (2012) On protein crowding and bilayer bulging in spontaneous vesicle formation. J Phys Chem B 116(42): 12677–12683

    Article  PubMed  CAS  Google Scholar 

  96. van Hoof B, Markvoort AJ, van Santen RA, Peter Hilbers AJ (2014) Molecular simulation of protein encapsulation in vesicle formation. J Phys Chem B 118(12):3346–3354

    Article  PubMed  CAS  Google Scholar 

  97. Schmidli PK, Schurtenberger P, Luisi PL (1991) Liposome-mediated enzymatic synthesis of phosphatidylcholine as an approach to self-replicating liposomes. J Am Chem Soc 113(21):8127–8130

    Article  CAS  Google Scholar 

  98. Liu AP, Fletcher DA (2009) Biology under construction: in vitro reconstitution of cellular function. Nat Rev Mol Cell Biol 10(9):644–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Endy D (2005) Foundations for engineering biology. Nature 438(7067):449–453

    Article  CAS  PubMed  Google Scholar 

  100. Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang R-Y, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi Z-Q, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA, 3rd, Smith HO, Venter JC (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329(5987):52–56

    Article  CAS  PubMed  Google Scholar 

  101. Hutchison CA, Chuang R-Y, Noskov VN, Assad-Garcia N, Deerinck TJ, Ellisman MH, Gill J, Kannan K, Karas BJ, Ma L, Pelletier JF, Qi Z-Q, Alexander Richter R, Strychalski EA, Sun L, Suzuki Y, Tsvetanova B, Wise KS, Smith HO, Glass JI, Merryman C, Gibson DG, Venter JC (2016) Design and synthesis of a minimal bacterial genome. Science 351(6280):aad6253

    Google Scholar 

  102. Damiano L, Hiolle A, Canamero L (2011) Grounding synthetic knowledge. In: Lenaerts T, Giacobini M, Bersini H, Bourgine P, Dorigo M, Doursat R (eds) Advances in artificial life, ECAL 2011. MIT press, Cambridge, pp 200–207

    Google Scholar 

  103. Dumouchel P, Damiano L (2017) Living with robots. Harvard University Press, Boston

    Google Scholar 

  104. Stano P, Luisi PL (2016) Theory and construction of semi-synthetic minimal cells. In: Nesbeth DN (ed) Synthetic biology handbook. CRC Press, pp 209–257

    Google Scholar 

  105. Luisi PL (1998) About various definitions of life. Orig Life Evol Biosph 28(4–6):613–622

    Article  CAS  PubMed  Google Scholar 

  106. Szostak JW (2012) Attempts to define life do not help to understand the origin of life. J Biomol Struct Dyn 29(4):599–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Varela FG, Maturana HR, Uribe R (1974) Autopoiesis: the organization of living systems, its characterization and a model. Biosystems 5(4):187–196

    Article  CAS  Google Scholar 

  108. Maturana HR, Varela FJ (1980) Autopoiesis and cognition: the realization of the living, 1st edn. D. Reidel Publishing Company

    Book  Google Scholar 

  109. Luisi PL (2003) Autopoiesis: a review and a reappraisal. Naturwissenschaften 90(2):49–59

    CAS  PubMed  Google Scholar 

  110. Bachmann PA, Walde P, Luisi PL, Lang J (1990) Self-replicating reverse micelles and chemical autopoiesis. J Am Chem Soc 112(22):8200–8201

    Article  CAS  Google Scholar 

  111. Bachmann PA, Luisi PL, Lang J (1992) Autocatalytic self-replicating micelles as models for prebiotic structures. Nature 357(6373):57–59

    Article  CAS  Google Scholar 

  112. Wick R, Walde P, Luisi PL (1995) Light-microscopic investigations of the autocatalytic self-reproduction of giant vesicles. J Am Chem Soc 117(4):1435–1436

    Article  CAS  Google Scholar 

  113. Luisi PL, Varela FJ (1989) Self-replicating micelles – a chemical version of a minimal autopoietic system. Orig Life Evol Biosph 19(6):633–643

    Article  CAS  Google Scholar 

  114. Stano P, Luisi PL (2010) Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem Commun (Camb) 46(21):3639–3653

    Article  CAS  Google Scholar 

  115. Luisi PL (1994) The chemical implementation of autopoiesis. In: Fleischaker GR, Colonna S, Luisi PL (eds) Self-production of supramolecular structures. From synthetic structures to models of minimal living systems. Number 446 in nato science series C, 1st edn. Kluver Academic Publisher, pp 197–179

    Google Scholar 

  116. Stano P (2010) Synthetic biology of minimal living cells: primitive cell models and semi-synthetic cells. Syst Synth Biol 4(3):149–156

    Article  PubMed  PubMed Central  Google Scholar 

  117. Haines TH (1983) Anionic lipid headgroups as a proton-conducting pathway along the surface of membranes – a hypothesis. Proc Natl Acad Sci USA 80(1):160–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Oberholzer T, Wick R, Luisi PL, Biebricher CK (1995) Enzymatic RNA replication in self-reproducing vesicles: an approach to a minimal cell. Biochem Biophys Res Commun 207(1):250–257

    Article  CAS  PubMed  Google Scholar 

  119. Dejanović B, Mirosavljević K, Noethig-Laslo V, Pecar S, Sentjurc M, Walde P (2008) An ESR characterization of micelles and vesicles formed in aqueous decanoic acid/sodium decanoate systems using different spin labels. Chem Phys Lipids 156(1–2):17–25

    Article  PubMed  CAS  Google Scholar 

  120. Stano P, Wehrli E, Luisi PL (2006) Insights into the self-reproduction of oleate vesicles. J Phys: Condens Matter 18(33):S2231

    CAS  Google Scholar 

  121. Chen IA, Szostak JW (2004) Membrane growth can generate a transmembrane pH gradient in fatty acid vesicles. Proc Natl Acad Sci USA 101(21):7965–7970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Budin I, Debnath A, Szostak JW (2012) Concentration-driven growth of model protocell membranes. J Am Chem Soc 134(51):20812–20819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Hentrich C, Szostak JW (2014) Controlled growth of filamentous fatty acid vesicles under flow. Langmuir 30(49):14916–14925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Kuruma Y, Stano P, Ueda T, Luisi PL (2009) A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim Biophys Acta 1788(2): 567–574

    Article  CAS  PubMed  Google Scholar 

  125. Scott A, Noga MJ, de Graaf P, Westerlaken I, Yildirim E, Danelon C (2016) Cell-free phospholipid biosynthesis by gene-encoded enzymes reconstituted in liposomes. PLoS ONE 11(10):e0163058

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  126. Peterlin P, Arrigler V, Kogej K, Svetina S, Walde P (2009) Growth and shape transformations of giant phospholipid vesicles upon interaction with an aqueous oleic acid suspension. Chem Phys Lipids 159(2):67–76

    Article  CAS  PubMed  Google Scholar 

  127. Takakura K, Toyota T, Sugawara T (2003) A novel system of self-reproducing giant vesicles. J Am Chem Soc 125(27):8134–8140

    Article  CAS  PubMed  Google Scholar 

  128. Kurihara K, Tamura M, Shohda K-I, Toyota T, Suzuki K, Sugawara T (2011) Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat Chem 3(10):775–781

    Article  CAS  PubMed  Google Scholar 

  129. Brea RJ, Cole CM, Devaraj NK (2014) In situ vesicle formation by native chemical ligation. Angew Chem Int Ed Engl 53(51):14102–14105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Deamer DW, Dworkin JP (2005) Chemistry and physics of primitive membranes. In: Walde P (ed) Prebiotic chemistry. Number 259 in topics in current chemistry. Springer, Berlin/Heidelberg, pp 1–27

    Google Scholar 

  131. Lawless JG, Zeitman B, Pereira WE, Summons RE, Duffield AM (1974) Dicarboxylic acids in the Murchison meteorite. Nature 251(5470):40–42

    Article  CAS  Google Scholar 

  132. Pizzarello S, Shock E (2010) The organic composition of carbonaceous meteorites: the evolutionary story ahead of biochemistry. Cold Spring Harb Perspect Biol 2(3):a002105

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  133. Gardner PM, Winzer K, Davis BG (2009) Sugar synthesis in a protocellular model leads to a cell signalling response in bacteria. Nat Chem 1(5):377–383

    Article  CAS  PubMed  Google Scholar 

  134. Chakrabarti AC, Breaker RR, Joyce GF, Deamer DW (1994) Production of RNA by a polymerase protein encapsulated within phospholipid vesicles. J Mol Evol 39(6):555–559

    Article  CAS  PubMed  Google Scholar 

  135. Oberholzer T, Albrizio M, Luisi PL (1995) Polymerase chain reaction in liposomes. Chem Biol 2(10):677–682

    Article  CAS  PubMed  Google Scholar 

  136. Mason JT, Xu L, Sheng Z-m, O’Leary TJ (2006) A liposome-PCR assay for the ultrasensitive detection of biological toxins. Nat Biotech 24(5):555–557

    Article  CAS  Google Scholar 

  137. Lee S, Koo H, Na JH, Lee KE, Jeong SY, Choi K, Kim SH, Kwon IC, Kim K (2014) DNA amplification in neutral liposomes for safe and efficient gene delivery. ACS Nano 8(5): 4257–4267

    Article  CAS  PubMed  Google Scholar 

  138. Oberholzer T, Nierhaus KH, Luisi PL (1999) Protein expression in liposomes. Biochem Biophys Res Commun 261(2):238–241

    Article  CAS  PubMed  Google Scholar 

  139. Chen IA, Salehi-Ashtiani K, Szostak JW (2005) RNA catalysis in model protocell vesicles. J Am Chem Soc 127(38):13213–13219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Anella F, Danelon C (2014) Reconciling ligase ribozyme activity with fatty acid vesicle stability. Life (Basel) 4(4):929–943

    CAS  Google Scholar 

  141. Gilbert W (1986) Origin of life: the RNA world. Nature 319(6055):618–618

    Article  Google Scholar 

  142. Gorlero M, Wieczorek R, Adamala K, Giorgi A, Schininà ME, Stano P, Luisi PL (2009) Ser-His catalyses the formation of peptides and PNAs. FEBS Lett 583(1):153–156

    Article  CAS  PubMed  Google Scholar 

  143. Luisi PL (2011) The synthetic approach in biology: epistemological notes for synthetic biology. In: Luisi PL, Chiarabelli C (eds) Chemical synthetic biology. Wiley, Chichester, pp 343–362

    Chapter  Google Scholar 

  144. Stano P, Carrara P, Kuruma Y, de Souza TP, Luisi PL (2011) 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

    Article  CAS  Google Scholar 

  145. Stano P, Luisi PL (2013) Semi-synthetic minimal cells: origin and recent developments. Curr Opin Biotechnol 24(4):633–638

    Article  CAS  PubMed  Google Scholar 

  146. Gil R, Silva FJ, Peret J, Moya A (2004) Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 68(3):518–537. Table of contents

    Google Scholar 

  147. Yu W, Sato K, Wakabayashi M, Nakaishi T, Ko-Mitamura EP, Shima Y, Urabe I, Yomo T (2001) Synthesis of functional protein in liposome. J Biosci Bioeng 92(6):590–593

    Article  CAS  PubMed  Google Scholar 

  148. Oberholzer T, Luisi PL (2002) The use of liposomes for constructing cell models. J Biol Phys 28(4):733–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, Nishikawa K, Ueda T (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19(8):751–755

    Article  CAS  PubMed  Google Scholar 

  150. Shimizu Y, Kanamori T, Ueda T (2005) Protein synthesis by pure translation systems. Methods 36(3):299–304

    Article  CAS  PubMed  Google Scholar 

  151. Hillebrecht JR, Chong S (2008) A comparative study of protein synthesis in in vitro systems: from the prokaryotic reconstituted to the eukaryotic extract-based. BMC Biotechnol 8:article no 58

    Google Scholar 

  152. Kita H, Matsuura T, Sunami T, Hosoda K, Ichihashi N, Tsukada K, Urabe I, Yomo T (2008) Replication of genetic information with self-encoded replicase in liposomes. Chembiochem 9(15):2403–2410

    Article  CAS  PubMed  Google Scholar 

  153. Hosoda K, Sunami T, Kazuta Y, Matsuura T, Suzuki H, Yomo T (2008) Quantitative study of the structure of multilamellar giant liposomes as a container of protein synthesis reaction. Langmuir 24(23):13540–13548

    Article  CAS  PubMed  Google Scholar 

  154. Ishikawa K, Sato K, Shima Y, Urabe I, Yomo T (2004) Expression of a cascading genetic network within liposomes. FEBS Lett 576(3):387–390

    Article  CAS  PubMed  Google Scholar 

  155. Shin J, Noireaux V (2012) An E. coli cell-free expression toolbox: application to synthetic gene circuits and artificial cells. ACS Synth Biol 1(1):29–41

    Article  CAS  PubMed  Google Scholar 

  156. Maeda YT, Nakadai T, Shin J, Uryu K, Noireaux V, Libchaber A (2012) Assembly of MreB filaments on liposome membranes: a synthetic biology approach. ACS Synth Biol 1(2):53–59

    Article  CAS  PubMed  Google Scholar 

  157. Soga H, Fujii S, Yomo T, Kato Y, Watanabe H, Matsuura T (2014) In vitro membrane protein synthesis inside cell-sized vesicles reveals the dependence of membrane protein integration on vesicle volume. ACS Synth Biol 3(6):372–379

    Article  CAS  PubMed  Google Scholar 

  158. Uyeda A, Nakayama S, Kato Y, Watanabe H, Matsuura T (2016) Construction of an in vitro gene screening system of the E. coli EmrE transporter using liposome display. Anal Chem 88(24):12028–12035

    Article  CAS  PubMed  Google Scholar 

  159. Hamada S, Tabuchi M, Toyota T, Sakurai T, Hosoi T, Nomoto T, Nakatani K, Fujinami M, Kanzaki R (2014) Giant vesicles functionally expressing membrane receptors for an insect pheromone. Chem Commun (Camb) 50(22):2958–2961

    Article  CAS  Google Scholar 

  160. Matsubayashi H, Kuruma Y, Ueda T (2014) In vitro synthesis of the E. coli sec translocon from DNA. Angew Chem Int Ed 53(29):7535–7538

    Article  CAS  Google Scholar 

  161. Stano P, Rampioni G, Francesca D’Angelo, Altamura E, Mavelli F, Marangoni R, Rossi F, Damiano L (2018) Current directions in synthetic cell research. In: Piotto S, Rossi F, Concilio S, Reverchon E, Cattaneo G (eds) Advances in bionanomaterials. Lecture notes in bioengineering. Springer, pp 141–154

    Google Scholar 

  162. Walker SA, Kennedy MT, Zasadzinski JA (1997) Encapsulation of bilayer vesicles by self-assembly. Nature 387(6628):61–64

    Article  CAS  PubMed  Google Scholar 

  163. Kisak ET, Coldren B, Evans CA, Boyer C, Zasadzinski JA (2004) The vesosome– a multicompartment drug delivery vehicle. Curr Med Chem 11(2):199–219

    Article  CAS  PubMed  Google Scholar 

  164. Paleos CM, Pantos A (2014) Molecular recognition and organizational and polyvalent effects in vesicles induce the formation of artificial multicompartment cells as model systems of eukaryotes. Acc Chem Res 47(5):1475–1482

    Article  CAS  PubMed  Google Scholar 

  165. Altamura E, Milano F, Tangorra RR, Trotta M, Hassan Omar O, Stano P, Mavelli F (2017) Highly oriented photosynthetic reaction centres generate a proton gradient in synthetic protocells. Proc Natl Acad Sci USA 114:3837–3842

    Article  CAS  PubMed  Google Scholar 

  166. Hadorn M, Eggenberger Hotz P (2010) DNA-mediated self-assembly of artificial vesicles. PLoS ONE 5(3):e9886

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  167. Hadorn M, Boenzli E, Sørensen KT, De Lucrezia D, Hanczyc MM, Yomo T (2013) Defined DNA-mediated assemblies of gene-expressing giant unilamellar vesicles. Langmuir 29(49):15309–15319

    Article  CAS  PubMed  Google Scholar 

  168. Cronin L, Krasnogor N, Davis BG, Alexander C, Robertson N, Steinke JHG, Schroeder SLM, Khlobystov AN, Cooper G, Gardner PM, Siepmann P, Whitaker BJ, Marsh D (2006) The imitation game–a computational chemical approach to recognizing life. Nat Biotechnol 24(10):1203–1206

    Article  CAS  PubMed  Google Scholar 

  169. Tomasi R, Noël J-M, Zenati A, Ristori S, Rossi F, Cabuil V, Kanoufi F, Abou-Hassan A (2014) Chemical communication between liposomes encapsulating a chemical oscillatory reaction. Chem Sci 5(5):1854–1859

    Article  CAS  Google Scholar 

  170. Liu Y, Wu H-C, Chhuan M, Terrell JL, Tsao C-Yu, Bentley WE, Payne GF (2015) Functionalizing soft matter for molecular communication. ACS Biomater Sci Eng 1(5):320–328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Liu Y, Tsao C-Yu, Kim E, Tschirhart T, Terrell JL, Bentley WE, Payne GF (2017) Using a redox modality to connect synthetic biology to electronics: hydrogel-based chemo-electro signal transduction for molecular communication. Adv Healthc Mater 6(1):article no 1600908

    Google Scholar 

  172. Nakano T, Moore M, Enomoto A, Suda T (2011) Molecular communication technology as a biological ICT. In: Sawai H (ed) Biological functions for information and communication technologies. Number 320 in studies in computational intelligence. Springer, Berlin/Heidelberg, pp 49–86

    Google Scholar 

  173. Nakano T, Eckford AW, Haraguchi T (2013) Molecular communications. Cambridge University Press, Cambridge

    Book  Google Scholar 

  174. Rampioni G, Damiano L, Messina M, D’Angelo F, Leoni L, Stano P (2013) Chemical communication between synthetic and natural cells: a possible experimental design. Electron Proc Theor Comput Sci 130:14–26

    Article  Google Scholar 

  175. Rampioni G, Mavelli F, Damiano L, DAngelo F, Messina M, Leoni L, Stano P (2014) A synthetic biology approach to bio-chem-ICT: first moves towards chemical communication between synthetic and natural cells. Nat Comput 13:1–17

    Article  CAS  Google Scholar 

  176. Lentini R, Santero SP, Chizzolini F, Cecchi D, Fontana J, Marchioretto M, Del Bianco C, Terrell JL, Spencer AC, Martini L, Forlin M, Assfalg M, Dalla Serra M, Bentley WE, Mansy SS (2014) Integrating artificial with natural cells to translate chemical messages that direct E. coli behaviour. Nat Commun 5:4012

    Google Scholar 

  177. Adamala KP, Martin-Alarcon DA, Guthrie-Honea KR, Boyden ES (2017) Engineering genetic circuit interactions within and between synthetic minimal cells. Nat Chem 9:431–439. Advance online publication

    Google Scholar 

  178. Lentini R, Martín NY, Forlin M, Belmonte L, Fontana J, Cornella M, Martini L, Tamburini S, Bentley WE, Jousson O, Mansy SS (2017) Two-way chemical communication between artificial and natural cells. ACS Cent Sci 3:117–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Shapiro L (2007) The embodied cognition research programme. Philos Compass 2:338–346

    Article  Google Scholar 

  180. Simon HA (1996) The sciences of the artificial. MIT Press, Cambridge

    Google Scholar 

  181. Bich L, Damiano L (2012) Life, autonomy and cognition: an organizational approach to the definition of the universal properties of life. Orig Life Evol Biosph 42:389–397

    Article  PubMed  Google Scholar 

  182. Damiano L, Kuruma Y, Stano P (2016) What can synthetic biology offer to artificial intelligence (and vice versa)? BioSystems 148:1–3

    Article  PubMed  Google Scholar 

  183. Eschenmoser A, Volkan Kisakuerek M (1996) Chemistry and the origin of life. Helv Chim Acta 79(5):1249–1259

    Article  Google Scholar 

Download references

Acknowledgements

The author is grateful to Pier Luigi Luisi (ETH Zürich, Switzerland and Uniroma3, Italy) for inspiring discussions over the past 15 years. Luisa Damiano (Univ. Messina and CERCO, Univ. of Bergamo) is acknowledged for the discussion presented in Sect. 6.5.2.1. Synthetic cell research has been developed with the framework of two European COST Actions, namely CM-1304 Emergence and Evolution of Complex Chemical Systems and TD-1308 Origins and evolution of life on Earth and in the Universe (ORIGINS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pasquale Stano .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Nature Singapore Pte Ltd.

About this chapter

Cite this chapter

Stano, P. (2017). Minimal Cellular Models for Origins-of-Life Studies and Biotechnology. In: Epand, R., Ruysschaert, JM. (eds) The Biophysics of Cell Membranes. Springer Series in Biophysics, vol 19. Springer, Singapore. https://doi.org/10.1007/978-981-10-6244-5_6

Download citation

Publish with us

Policies and ethics