title: Escalation of polymerization in a thermal gradient.
abstract: For the emergence of early life, the formation of biopolymers such as RNA is essential. However, the addition of nucleotide monomers to existing oligonucleotides requires millimolar concentrations. Even in such optimistic settings, no polymerization of RNA longer than about 20 bases could be demonstrated. How then could self-replicating ribozymes appear, for which recent experiments suggest a minimal length of 200 nt? Here, we demonstrate a mechanism to bridge this gap: the escalated polymerization of nucleotides by a spatially confined thermal gradient. The gradient accumulates monomers by thermophoresis and convection while retaining longer polymers exponentially better. Polymerization and accumulation become mutually self-enhancing and result in a hyperexponential escalation of polymer length. We describe this escalation theoretically under the conservative assumption of reversible polymerization. Taking into account the separately measured thermophoretic properties of RNA, we extrapolate the results for primordial RNA polymerization inside a temperature gradient in pores or fissures of rocks. With a dilute, nanomolar concentration of monomers the model predicts that a pore length of 5 cm and a temperature difference of 10 K suffice to polymerize 200-mers of RNA in micromolar concentrations. The probability to generate these long RNAs is raised by a factor of >10(600) compared with polymerization in a physical equilibrium. We experimentally validate the theory with the reversible polymerization of DNA blocks in a laser-driven thermal trap. The results confirm that a thermal gradient can significantly enlarge the available sequence space for the emergence of catalytically active polymers.
authors: Systems Biophysics, Physics Department, Center for Nanoscience, Ludwig-Maximilians-Universität München, 80799 Munich, Germany.
authors: Christof B
authors: CB
authors: Mast
authors: Severin
authors: S
authors: Schink
authors: Ulrich
authors: U
authors: Gerland
authors: Dieter
authors: D
authors: Braun
mesh_terms: D001704:Biopolymers / Q000737:chemistry*; D002138:Calibration; D002384:Catalysis; D004247:DNA / Q000737:chemistry; D031541:Fluorescence Resonance Energy Transfer; D005844:Geology / Q000379:methods; D007700:Kinetics; D015233:Models, Statistical; D009711:Nucleotides / Q000737:chemistry; D058105:Polymerization; D012313:RNA / Q000737:chemistry*; D016337:RNA, Catalytic / Q000737:chemistry*; D013696:Temperature; D014867:Water / Q000737:chemistry
chemical_list: D001704:Biopolymers; D009711:Nucleotides; D016337:RNA, Catalytic; D014867:Water; D012313:RNA; D004247:DNA
keywords: (nonenzymatic) emergence of RNA; RNA world; hydrothermal vents; molecular evolution; nonequilibrium
references: Chem Soc Rev. 2012 Aug 21;41(16):5526-65
references: 22684046
references: Proc Natl Acad Sci U S A. 2007 May 29;104(22):9346-51
references: 17494767
references: Proc Natl Acad Sci U S A. 1965 Sep;54(3):919-27
references: 5217468
references: Nature. 1970 Aug 8;227(5258):561-3
references: 4913914
references: J Am Chem Soc. 2009 Feb 25;131(7):2422-3
references: 19193012
references: Astrobiology. 2011 Dec;11(10):933-50
references: 22111762
references: Nano Lett. 2009 Dec;9(12):4264-7
references: 19807065
references: Phys Rev Lett. 2002 Oct 28;89(18):188103
references: 12398641
references: Langmuir. 2007 Feb 13;23(4):1674-83
references: 17279644
references: Proc Natl Acad Sci U S A. 2010 Mar 9;107(10):4585-9
references: 20176971
references: Proc Natl Acad Sci U S A. 2011 May 31;108(22):9049-54
references: 21562213
references: Phys Rev Lett. 2012 Jun 8;108(23):238104
references: 23003995
references: Phys Rev Lett. 2003 Oct 10;91(15):158103
references: 14611502
references: Angew Chem Int Ed Engl. 2010 Oct 18;49(43):7948-51
references: 20836102
references: Science. 2009 Feb 27;323(5918):1229-32
references: 19131595
references: Phys Rev Lett. 2011 Jul 1;107(1):018101
references: 21797574
references: Nature. 1996 May 2;381(6577):59-61
references: 8609988
references: J Am Chem Soc. 2012 Feb 29;134(8):3691-4
references: 22296305
references: J Am Chem Soc. 2009 Jul 22;131(28):9628-9
references: 19601679
references: Phys Rev Lett. 2010 May 7;104(18):188102
references: 20482214
references: Science. 2011 Apr 8;332(6026):209-12
references: 21474753
references: J Phys Chem B. 2012 Jun 28;116(25):7463-9
references: 22663072
references: Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9516-21
references: 18606997
references: Electrophoresis. 2010 Jan;31(2):279-86
references: 20084627
references: Proc Natl Acad Sci U S A. 2012 Apr 24;109(17):6405-10
references: 22493232
references: Nat Rev Microbiol. 2008 Nov;6(11):805-14
references: 18820700
references: Angew Chem Int Ed Engl. 2012 Oct 15;51(42):10656-9
references: 23001866
references: Chembiochem. 2012 May 7;13(7):999-1008
references: 22474011
references: Phys Rev Lett. 2006 Jul 21;97(3):038103
references: 16907547
references: Proc Natl Acad Sci U S A. 2006 Dec 26;103(52):19678-82
references: 17164337
references: J Biol Chem. 2009 Nov 27;284(48):33206-16
references: 19801553