Skip to main content

RNA as Major Components in Chemical Evolvable Systems

  • Chapter
  • First Online:
Chemical Biology of Nucleic Acids

Part of the book series: RNA Technologies ((RNATECHN))

Abstract

A milestone for the origin of life was the onset of a sustained functional interplay between nucleic acids, peptides, lipids and sugars, to form chemical dynamic off-equilibrium systems. The bilayer surface of lipidic vesicles served for the anchoring and enrichment of macromolecules that could grow in size would interact with one another one thousand fold more frequently than unbound in solution and could sooner or later be internalised into the interior of the vesicles. Within a flow of exogenous high-energy compounds, internalised, possibly surface-bound, hereditary molecules like RNA could then grow in population size and length more rapidly, safer and more reliably. When “fed” with activated and activating monomers over a long enough time period, such systems would persist, acquire partial control over their environment and eventually produce replicating protocells capable of autonomously producing high-energy compounds on their own.

We are outlining here how hydrophobic interactions between peptides and lipids can drive supramolecular multicomponent systems including RNA to assemble into models of functionalised protocells that carry potentially inheritable genetic information. Mixing chemically activated macromolecular libraries of synthetic biomolecules with an evolvable population of lipidic giant vesicles is an experimental bottom-up approach being rooted in a growing community of the emergent research area “Systems Chemistry”. The aim of such experimentation is to initiate lifelike behaviour from inanimate chemical systems. The impact of having at one’s disposal chemical protocols for the off-equilibrium search for synthetic peptides that transport synthetic RNA into giant lipidic vesicles (or cells) is difficult to overestimate. On a fundamental level, the impact of being able to prepare “living synthetic cells” would be quite breathtaking.

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 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

Notes

  1. 1.

    Old Swiss saying: Das schläggt kei Geiss ewägg, something like: no goat can lick this off !

References

  • Acosta-Silva C, Bertran J, Branchadell V et al (2012) Quantum-mechanical study on the mechanism of peptide bond formation in the ribosome. J Am Chem Soc 134:5817–5831

    Article  CAS  PubMed  Google Scholar 

  • Allen W (2009) Whatever works, comedy, 92 minutes. Sony Pictures Classics, USA

    Google Scholar 

  • Apel CL, Deamer DW (2005) The formation of glycerol monodecanoate by a dehydration condensation reaction: increasing the chemical complexity of amphiphiles on the early Earth. Orig Life Evol Biosph 35:323–332

    Article  CAS  PubMed  Google Scholar 

  • Attwater J, Wochner A, Holliger P (2013) In-ice evolution of RNA I polymerase ribozyme activity. Nat Chem 5:1011–1018

    Article  CAS  PubMed  Google Scholar 

  • Benner SA, Kim H-J, Carrigan MA (2012) Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc Chem Res 45:2025–2034

    Article  CAS  PubMed  Google Scholar 

  • Biała E, Strazewski P (2002) Internally mismatched RNA: pH and solvent dependence of the thermal unfolding of tRNAAla acceptor stem microhairpins. J Am Chem Soc 124:3540–3545

    Article  PubMed  Google Scholar 

  • Briers Y, Stäubli T, Schmid MC et al (2012a) Intracellular vesicles as reproduction elements in cell wall-deficient L-form bacteria. PLoS One 7:e38514

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Briers Y, Walde P, Schuppler M et al (2012b) How did bacterial ancestors reproduce? Lessons from L-form cells and giant lipid vesicles. Bioesssays 34:1078–1084

    Article  CAS  Google Scholar 

  • Budin I, Szostak JW (2011) Physical effects underlying the transition from primitive to modern cell membranes. Proc Natl Acad Sci U S A 108:5249–5525

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cech T (2012) The RNA world’s in context. Cold Spring Harb Perspect Biol 4:a006742

    Article  PubMed  Google Scholar 

  • Coleman A, Lazar A, Terenzi S et al (2006) Observation of the formation of supported bilayers by amphiphilic peptidyl-RNA. Chem Commun (1):63–65

    Google Scholar 

  • Deck C, Jauker M, Richert C (2011) Efficient enzyme-free copying of all four nucleobases templated by immobilized RNA. Nat Chem 3:603–608

    Article  CAS  PubMed  Google Scholar 

  • DeMarco ML (2012) Three-dimensional structure of glycolipids in biological membranes. Biochemistry 51:5725–5732

    Article  CAS  PubMed  Google Scholar 

  • Derossi D, Chassaing G, Prochiantz A (1998) Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol 8:84–87

    Article  CAS  PubMed  Google Scholar 

  • Dupont E, Prochiantz A, Joliot A (2011) Penetratin story: an overview. Methods Enzymol 683:21–29

    CAS  Google Scholar 

  • Elias HG (1997) An introduction to polymer science. VCH, Weinheim

    Google Scholar 

  • Ellington A (2012) Origins for everyone. Evol Educ Outreach 5:361–366

    Article  Google Scholar 

  • Harland CW, Botyanszki Z, Rabuka D, Bertozzi CR, Parthasarathy R (2009) Synthetic trehalose glycolipids confer desiccation resistance to supported lipid monolayers. Langmuir 25:5193–5198

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hawking S (2001) The universe in a nutshell. Bantam, London

    Google Scholar 

  • Hein JE, Blackmond DG (2012) On the origin of single chirality of amino acids and sugars in biogenesis. Acc Chem Res 45:2045–2054

    Article  CAS  PubMed  Google Scholar 

  • Hill AR Jr, Orgel L (1996) Oligomerization of negatively-charged amino acids by carbonyldiimidazole. Orig Life Evol Biosph 26:539–545

    Article  CAS  PubMed  Google Scholar 

  • Iordache O (2012) Self-evolvable systems. Understanding complex systems. Springer, Heidelberg. ISBN 978-3-642-28881-4

    Book  Google Scholar 

  • Järver P, Coursindel T, Andaloussi SEL et al (2011) Peptide-mediated cell and in vivo delivery of antisense oligonucleotides and siRNA. Mol Ther Nucleic Acids 1:e27

    Article  Google Scholar 

  • Kauffman S (2000) Investigations. Oxford University Press, New York

    Google Scholar 

  • Keller RCA, Killian JA, de Kruijff B (1992) Anionic phospholipids are essential for α-helix formation of the signal peptide of prePhoE upon interaction with phospholipid vesicles. Biochemistry 31:1672–1677

    Article  CAS  PubMed  Google Scholar 

  • Kol MA, van Laak AN, Rijkers DT et al (2003) Phospholipid flop induced by transmembrane peptides in model membranes is modulated by lipid composition. Biochemistry 42:231–237

    Article  CAS  PubMed  Google Scholar 

  • Kooijman EE, Carter KM, van Laar EG et al (2005) What makes the bioactive lipids phosphatidic acid and lysophosphatidic acid so special? Biochemistry 44:17007–17015

    Article  CAS  PubMed  Google Scholar 

  • Kooijman EE, Tieleman DP, Testerink C et al (2007) An electrostatic/hydrogen bond switch as the basis for the specific interaction of phosphatidic acid with proteins. J Biol Chem 282:11356–11364

    Article  CAS  PubMed  Google Scholar 

  • Lamazière A, Wolf C, Lambert O et al (2008) The homeodomain derived peptide Penetratin induces curvature of fluid membrane domains. PLoS One 3:e1938

    Article  PubMed Central  PubMed  Google Scholar 

  • Lamy C, Lemoine J, Bouchu D et al (2008) Glutamate-glycine and histidine-glycine co-oligopeptides: batch co-oligomerization versus pulsed addition of N-carboxyanhydrides. Chembiochem 9:710–713

    Article  CAS  PubMed  Google Scholar 

  • Le Chevalier Isaad A, Carrara P, Stano P et al (2014) A hydrophobic peptide anchors RNA to giant lipidic vesicles. Org Biomol Chem (in press)

    Google Scholar 

  • Lehman N (2013) Cold-hearted RNA heats up life. Nat Chem 5:987–989

    Article  CAS  PubMed  Google Scholar 

  • Li W, Nicol F, Szoka FC Jr (2004) GALA: a designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv Drug Deliv Rev 56:967–985, and references therein

    Article  CAS  PubMed  Google Scholar 

  • Luisi PL (2006) The emergence of life. From chemical origins to synthetic biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Luther A, Brandsch R, von Kiedrowski G (1998) Surface-promoted replication and exponential amplification of DNA analogues. Nature 396:245–248

    Article  CAS  PubMed  Google Scholar 

  • Lynn D, Burrows C, Goodwin J et al (2012) Origins of chemical evolution. Acc Chem Res 45:2023–2024

    Article  CAS  PubMed  Google Scholar 

  • Magritte R (1929) La Trahison des images, huile sur toile, 59 × 65 cm. Art Institute of Chicago, Los Angeles

    Google Scholar 

  • Mansy SS, Schrum JP, Krishnamurthy M et al (2008) Template-directed synthesis of a genetic polymer in a model protocell. Nature 454:122–125

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maurer SE, Deamer DW, Boncella JM et al (2009) Chemical evolution of amphiphiles: glycerol monoacyl derivatives stabilize plausible prebiotic membranes. Astrobiology 9:979–987

    Article  CAS  PubMed  Google Scholar 

  • Meierhenrich UJ, Filippi J-J, Meinert C et al (2010) On the origin of primitive cells: from nutrient intake to elongation of encapsulated nucleotides. Angew Chem Int Ed 49:3738–3750

    Article  CAS  Google Scholar 

  • Midoux P, LeCam E, Coulaud D et al (2003) Histidine containing peptides and polypeptides as nucleic acid vectors. In: Luo D, Saltzman WC (eds) Synthetic DNA delivery systems. Kluwer Academic/Plenum, London, pp 23–44

    Google Scholar 

  • Nyholm TMK, Özdirekcan S, Killian JA (2007) How protein transmembrane segments sense the lipid environment. Biochemistry 46:1457–1465

    Article  CAS  PubMed  Google Scholar 

  • Pascal R, Boiteau L, Commeyras A (2005) From the prebiotic synthesis of alpha-amino acids towards a primitive translation apparatus for the synthesis of peptides. Top Curr Chem 259:69–122

    Article  CAS  Google Scholar 

  • Plank P, Oberhauser B, Mechtler K et al (1994) The influence of endosome-disruptive peptides on gene transfer using synthetic virus-like gene transfer systems. J Biol Chem 269:12918–12924

    CAS  PubMed  Google Scholar 

  • Pross A (2012) What is life? How chemistry becomes biology. Oxford University Press, Oxford

    Google Scholar 

  • Raja M, Spelbrink RE, de Kruijff B et al (2007) Phosphatidic acid plays a special role in stabilizing and folding of the tetrameric potassium channel KcsA. FEBS Lett 581:5715–5722

    Article  CAS  PubMed  Google Scholar 

  • Rushdi A, Simoneit BRT (2006) Abiotic condensation synthesis of glyceride lipids and wax esters under simulated hydrothermal conditions. Orig Life Evol Biosph 36:93–108

    Article  CAS  PubMed  Google Scholar 

  • Speelmans G, Staffhorst RWHM, de Kruijff B (1997) The anionic phospholipid-mediated membrane interaction of the anti-cancer drug doxorubicin is enhanced by phosphatidylethanolamine compared to other zwitterionic phospholipids. Biochemistry 36:8657–8662

    Article  PubMed  Google Scholar 

  • Strazewski P (2009) Adding to Hans Kuhn’s thesis on the emergence of the genetic apparatus: of the Darwinian advantage to be neither too soluble, nor too insoluble, neither too solid, nor completely liquid. Colloids Surf B Biointerfaces 74:419–425

    Article  CAS  PubMed  Google Scholar 

  • Strazewski P (2014) Amphiphilic peptidyl-RNA. In: Stulz E, Clever GH (eds) DNA in supramolecular chemistry and nanotechnology. Wiley, New York

    Google Scholar 

  • Subramanian AB, Guidotti G, Manoharan VN et al (2013) Glycans pattern the phase behaviour of lipid membranes. Nat Mat 12:128–133

    Article  Google Scholar 

  • Szathmáry E (2006) The origin of replicators and reproducers. Phil Trans R Soc Lond B Biol Sci 361:1761–1776

    Article  Google Scholar 

  • Taillades J, Cottet H, Garrel L et al (1999) N-carbamoyl amino acid solid-gas nitrosation by NO/NOx: a new route to oligopeptides via alpha-amino acid N-carboxyanhydride. Prebiotic implications. J Mol Evol 48:638–645

    Article  CAS  PubMed  Google Scholar 

  • Terenzi S, Biała E, Nguyen-Trung NQ et al (2003) Amphiphilic 3′-peptidyl-RNA conjugates. Angew Chem Int Ed 42:2909–2912

    Article  CAS  Google Scholar 

  • van Klompenburg W, Nilsson IM, von Heijne G et al (1997) Anionic phospholipids are determinants of membrane protein topology. EMBO J 16:4261–4266

    Article  PubMed Central  PubMed  Google Scholar 

  • von Kiedrowski G, Herdewijn P, Otto S (2010) Welcome home system chemists! J Syst Chem 1:1

    Article  Google Scholar 

  • von Trier L, Vinterberg T, Levring K et al (1995) Dogme 95, Denmark

    Google Scholar 

  • Wimley WC, White SH (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3:842–848

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Zang S, Chaput JC (2012) Darwinian evolution of an alternative genetic system provides support for TNA as an RNA progenitor. Nat Chem 4:183–187

    Article  CAS  PubMed  Google Scholar 

  • Zaccai NR, Chi B, Thomson AR et al (2011) A de novo peptide hexamer with a mutable channel. Nat Chem Biol 7:935–941

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S (2012) Lipid-like self-assembling peptides. Acc Chem Res 45:2142–2150

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work would never have been possible without the devoted action of a number of colleagues and collaborators, in particular, Oliver Botta, Ewa Biała, Silvia Terenzi, Nhat Quang Nguyen Trung, Carole Lamy, Peter Goekjian, Denis Bouchu, Alexandra Le Chevalier Isaad, Krishnakumar KS, Pasquale Stano, Paolo Carrara, René Buchet, Dominique Lafont, and Florian Albrieux. Discussions over the years with Günter von Kiedrowski, Eörs Szathmáry, Pier Luigi Luisi, Albert Eschenmoser, Hans Kuhn, Stuart Kauffman, and Addy Pross have moulded on my way of thinking about le monde vivant into what it has become now; my deepest thanks to all these scientists. The financial support from the 6th European Framework Programme in Synthetic Biology for the research programme “Synthcells” (contract no. 043359) and from the European Coordination of Science and Technology Action on “Systems Chemistry” (COST Action CM0703) is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter Strazewski .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Strazewski, P. (2014). RNA as Major Components in Chemical Evolvable Systems. In: Erdmann, V., Markiewicz, W., Barciszewski, J. (eds) Chemical Biology of Nucleic Acids. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54452-1_1

Download citation

Publish with us

Policies and ethics