The RNA World: Molecular cooperation at the origins of life

Nature Reviews Genetics

Volumn 16, Issue 1, 2015, Pages 7-17

  Higgs, Paul G ^a   Lehman, Niles ^a,b  

^a MCMASTER UNIVERSITY   (Canada)

^b PORTLAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PREBIOTIC AGENT; RNA; RNA POLYMERASE; RIBOZYME;

BIOGENESIS; CATALYSIS; COLD; COOPERATION; COVALENT BOND; DNA REPLICATION; GENOTYPE; HISTORY OF MEDICINE; MICROENVIRONMENT; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NUCLEOTIDE METABOLISM; PHENOTYPE; POLYMERIZATION; PRIORITY JOURNAL; REVIEW; RNA REPLICATION; RNA SEQUENCE; RNA SYNTHESIS; RNA TRANSCRIPTION; BASE PAIRING; BIOLOGICAL MODEL; BIOSYNTHESIS; GENETICS; METABOLISM; PHYSIOLOGY;

BASE PAIRING; BIOGENESIS; EVOLUTION, MOLECULAR; MODELS, BIOLOGICAL; RNA; RNA, CATALYTIC;

EID: 84926186318     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3841     Document Type: Review

References (120)

1. Crick, F. H. C. The origin of the genetic code. J. Mol. Biol. 38, 367-379 (1968).
2. Orgel, L. E. Evolution of the genetic apparatus. J. Mol. Biol. 38, 381-393 (1968).
3. White, H. B. Coenzymes as fossils of an earlier metabolic state. J. Mol. Evol. 7, 101-104 (1976).
4. Kruger, K. et al. Self-splicing RNA: autoexcisionand autocyclization of the ribosomal RNA interveningsequence of Tetrahymena. Cell 31, 147-157 (1982).
5. Guerrier-Takada, C. et al. The RNA moiety of ribonuclease P is thecatalytic subunit of the enzyme. Cell 35, 849-857 (1983).
6. Nissan, P., Hansen, J., Ban, N., Moore, P. B. & Steitz, T. A. The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920-930 (2000).
7. Mills, D. R., Peterson, R. L. & Spiegelman, S. An extracellular darwinian evolution experiment with a self-duplicating nucleic acid molecule. Proc. Natl Acad. Sci. USA 58, 217-224 (1967).
8. Joyce, G. F. Forty years of in vitro evolution. Angew. Chem. Int. Ed. 46, 6420-6436 (2007).
9. Biebricher, C. K. & Orgel, L. E. An RNA that multiplies indefinitely with DNA-dependent RNA polymerase: selection from a random copolymer. Proc. Natl Acad. Sci. USA 70, 934-938 (1973).
10. Biebricher, C. K., Eigen, M, & Gardiner, W. C. Kinetics of RNA replication: competition and selection among self-replicating RNA species. Biochemistry 24, 6550-6560 (1985).
11. Robertson, D. L. & Joyce, G. F. Selection in vitro of an RNA enzyme that specifically cleaves singlestranded DNA. Nature 344, 467-468 (1990).
12. Beaudry, A. A. & Joyce, G. F. Directed evolution of an RNA enzyme. Science 257, 635-641 (1992).
13. Tuerk, C. & Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510 (1990).
14. Ellington, A. D. & Szostak, J. W. In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822 (1990).
15. Chen, X., Li, N. & Ellington, A. D. Ribozyme catalysis of metabolism in the RNA world. Chem. Biodivers. 4, 633-655 (2007).
16. Mandal, R. & Breaker, R. R. Gene regulation byriboswitches. Nature Rev. Mol. Cell. Biol. 5, 451-463 (2004).
17. Lincoln, T. A. & Joyce, G. F. Self-sustained replication of an RNA enzyme. Science 323, 1229-1232 (2009).
18. 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).
19. Zaher, H. S. & Unrau, P. J. Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA 13, 1017-1026 (2007).
20. Cheng, L. K. L. & Unrau, P. J. Closing the circle: replicating RNA with RNA. Cold Spring Harb. Perspect. Biol. 2, a002204 (2010).
21. Shapiro, R. Origins: A Skeptic's Guide to the Creation of Life on Earth (Bantam New Age,1987).
22. Shapiro, R. A simpler origin of life. Sci. Am. 296, 46-53 (2007).
23. Neveu, M., Kim, H. J. & Benner, S. A. The "strong" RNA world hypothesis: fifty years old. Astrobiology 13, 391-403 (2013).
24. Joyce, G. F., Schwartz, A. W., Miller, S. L. & Orgel, L. E. The case for an ancestral genetic system involving simple analogues of the nucleotides. Proc. Natl Acad. Sci. USA 84, 4398-4402 (1987).
25. Joyce, G. F. The rise and fall of the RNA world. New Biol. 3, 399-407 (1991).
26. Joyce, G. F. The antiquity of RNA-based evolution. Nature 418, 214-221 (2002).
27. Benner, S. A., Kim, H.J. & Carrigan, M. A. Asphalt, water, and the prebiotic synthesis of ribose, ribonucleotides, and RNA. Acc. Chem. Res. 45, 2025-2034 (2012).
28. Ricardo, A., Carrigan, M. A., Olcott, A. & Benner, S. A. Borate minerals stabilize ribose. Science 303,196 (2004).
29. Vázquez-Mayagoitia, A. et al. On the stabilization of ribose by silicate minerals. Astrobiology 11, 115-121 (2011).
30. Anastasi, C. et al. RNA: prebiotic product, or biotic invention? Chem. Biodivers. 4, 721-739 (2007).
31. Powner, M. W., Gerland, B. & Sutherland, J. D. Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459, 239-242 (2009).
32. Pasek, M. A., Harnmeijer, J. P., Buick, R., Gull, M. & Atlas, Z. Evidence for reactive reduced phosphorus species in the early Archaen ocean. Proc. Natl Acad. Sci. USA 110, 10089-10094 (2013).
33. Ritson, D. & Sutherland, J. D. Prebiotic synthesis of simple sugars by photoredox systems chemistry. Nature Chem. 4, 895-899 (2012).
34. Bowler, F. R. et al. Prebiotically plausible oligoribonucleotide ligation facilitated by chemoselective acetylation. Nature Chem. 5, 383-389 (2013).
35. Wächtershäuser, G. Before enzymes and templates: theory of surface metabolism. Microbiol. Rev. 52, 452-484 (1988).
36. Orgel, L. E. Did template-directed nucleation precede molecular replication? Orig. Life Evol. Biosph. 17, 27-34 (1986).
37. Ferris, J. P. Mineral catalysis and prebiotic synthesis: montmorillonite-catalyzed formation of RNA. Elements 1, 145-149 (2005).
38. Monnard, P.-A., Kanavarioti, A. & Deamer, D. W. Eutectic phase polymerization of activated ribonucleotide mixtures yields quasi-equimolar incorporation of purine and pyrimidine nucleobases. J. Am. Chem. Soc. 125, 13734-13740 (2003).
39. Monnard, P.-A. & Szostak, J. W. Metal-ion catalyzed polymerization in the eutectic phase in water-ice: a possible approach to template-directed RNA polymerization J. Inorg. Biochem. 102, 1104-1111 (2008).
40. Cafferty, B. J. et al. Efficient self-assembly in water of long noncovalent polymers by nucleobases analogs. J. Am. Chem. Soc. 135, 2447-2450 (2013).
41. Kuruvilla, E., Schuster, G. B. & Hud, N. V. Enhanced nonenzymatic ligation of homopurine miniduplexes: support for greater base stacking in a pre-RNA world. ChemBioChem 14, 45-48 (2013).
42. Hud, N. V., Cafferty, B. J., Krishnamurthy, R. & Williams, L. D. The origin of RNA and "my grandfather's axe". Chem. Biol. 20, 466-474 (2013).
43. Wu, T. & Orgel, L. E. Nonenzymatic template-directed synthesis on oligodeoxycytidylate sequences in hairpin oligonucleotides. J. Am. Chem. Soc. 114, 317-322 (1992).
44. Hill, A. R. Jr., Wu, T. & Orgel, L. E. The limits of template-directed synthesis with nucleoside-5-phosph oro(2-methyl)imidazolides. Origins Life Evol. Biosph. 23, 285-290 (1993).
45. Deck, C., Jauker, M. & Richert, C. Efficient enzyme-free copying of all four nucleobases templated by immobilized RNA. Nature Chem. 3, 603-608 (2011).
46. Lehman, N. & Hayden, E. J. Template-directed RNA polymerization: the taming of the milieu. ChemBioChem 12, 2727-2728 (2011).
47. Moulton, V. et al. RNA folding argues against a hot-start origin of life. J. Mol. Evol. 51, 416-421 (2000).
48. Vlassov, A. V., Johnston, B. H., Landweber, L. F. & Kazakov, S. A. Ligation activity of fragmented ribozymes in frozen solution: implications for the RNA world. Nucleic Acids Res. 25, 2966-2974 (2004).
49. Wochner, A., Attwater, J., Coulson, A. & Holliger, P. Ribozyme-catalyzed transcription of an active ribozyme. Science 332, 209-212 (2011).
50. Attwater, J., Wochner, A. & Holliger, P. In-ice evolution of RNA polymerase ribozyme activity. Nature Chem. 5, 1011-1018 (2013).
51. Lehman, N. Cold-hearted RNA heats up life. Nature Chem. 5, 987-989 (2011).
52. Huang, W. & Ferris, J. P. One-step, regioselective synthesis of up to 50-mers of RNA oligomers by montmorillonite catalysis. J. Am. Chem. Soc. 128, 8914-8919 (2006).
53. Kauffman, S. A. The Origins of Order: Self-Organization and Selection in Evolution (Oxford Univ. Press, 1993).
54. Hordijk, W. & Steel, M. Detecting autocatalytic, self-containing sets in chemical reaction systems. J. Theor. Biol. 227, 451-461 (2004).
55. Hordijk, W. & Steel, M. A formal model of autocatalytic sets emerging in a RNA replicator system. J. Syst. Chem.4, 3 (2013).
56. Smith, J. I., Steel, M. & Hordijk, W. Autocatalytic sets in a partitioned chemical network. J. Syst. Chem. 5, 2 (2014).
57. Hayden, E. J. & Lehman, N. Self-assembly of a group I intron from inactive oligonucleotide fragments. Chem. Biol. 13, 909-918 (2006).
58. Hayden, E. J., von Kiedrowski, G. & Lehman, N. Systems chemistry on ribozyme self-construction: Evidence for anabolic autocatalysis in a recombination network. Angew. Chem. Int. Ed. 47, 8424-8428 (2008).
59. Burton, A. S. & Lehman, N. Enhancing the prebiotic relevance of a set of covalently self-assembling, autorecombining RNAs through in vitro selection. J. Mol. Evol. 70, 233-241 (2010).
60. Vaidya, N. et al. Spontaneous network formation among cooperative RNA replicators. Nature 491, 72-77 (2012).
61. Vaidya, N., Walker, S. I. & Lehman, N. Recycling of informational units leads to selection of replicators in a prebiotic soup. Chem. Biol. 20, 241-252 (2013).
62. Levy, M. & Ellington, A. D. The descent of polymerization. Nature Struct. Biol. 8, 580-582 (2001).
63. Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution (Oxford University Press,1995).
64. Hammerstein, P. Genetic and Cultural Evolution of Cooperation (MIT Press, 2003).
65. Nowak, M. A. Five rules for the evolution of cooperation. Science 314, 1560-1563 (2006).
66. Boerlijst, M. C. & Hogeweg, P. Spiral wave structure in prebiotic evolution: hypercycles stable against parasites. Physica. D 48, 17-28 (1991).
67. Sardanyes, J. & Solé, R. V. Bifurcations and phase transitions in spatially extended two-member hypercycles. J. Theor. Biol. 243, 468-482 (2006).
68. Sardanyes, J. & Solé, R. V. Spatiotemporal dynamics in simple asymmetric hypercycles under weak parasitic coupling. Physica. D 231, 116-129 (2007).
69. McCaskill, J. S., Füchslin, R. M. & Altmeyer, S. The stochastic evolution of catalysts in spatially resolved molecular systems. Biol. Chem. 382, 1343-1363 (2001).
70. Konnyu, B., Czaran, T. & Szathmáry, E. Prebiotic replicase evolution in a surface-bound metabolic system: parasites as a source of adaptive evolution. BMC Evol. Biol. 8, 267 (2008).
71. Branciamore, S., Gallori, E., Szathmáry, E. & Czaran, T. The origin of life: chemical evolution of a metabolic system in a mineral honeycomb? J. Mol. Evol. 69, 485-469 (2009).
72. Brogioli, D. Marginally stable chemical systems as precursors for life. Phys. Rev. Lett. 105, 058102 (2010).
73. Szabo, P., Scheuring, I., Czaran, T. & Szathmáry, E. In silico simulations reveal that replicators with limited dispersal evolve towards higher efficiency and fidelity. Nature 420, 340-343 (2002).
74. Eigen, M. & Schuster, P. The hypercycle: a principle of natural self-organization. Part B: the abstract hypercycle. Naturwissenschaften 65, 7-41 (1978).
75. Eigen, M., McCaskill, J. & Schuster, P. Molecular quasi-species. J. Phys. Chem. 92, 6881-6891 (1988).
76. Takeuchi, N. & Hogeweg, P. Evolutionary dynamics of RNA-like replicator systems: a bioinformatic approach to the origin of life. Phys. Life Rev. 9, 219-263 (2012).
77. Takeuchi, N. & Hogeweg, P. The role of complex formation and deleterious mutations for the stability of RNA-like replicator systems. J. Mol. Evol. 65, 668-686 (2007).
78. Wu, M. & Higgs, P. G. The origin of life is a spatially localized stochastic transition. Biol. Direct 7, 42 (2012).
79. Higgs, P. G. & Wu, M. The importance of stochastic transitions for the origin of life. Orig. Life Evol. Biosph. 42, 453-457 (2012).
80. Takeuchi, N. & Hogeweg, P. Evolution of complexity in RNA-like replicator systems. Biol. Direct 3,11 (2008).
81. Takeuchi, N. Salazar, L., Poole, A. M. & Hogeweg, P. The evolution of strand preference in simulated RNA replicators with strand displacement: implications for the origin of transcription. Biol. Direct. 3, 33 (2008).
82. Shay, J. A., Huynh, C. & Higgs, P. G. The origin and spread of a cooperative replicase in a prebiotic chemical system. J. Theor. Biol. http://dx.doi. org/10.1016/j.jtbi.2014.09.019 (2014).
83. Szathmáry, E. & Demeter, L. Group selection of early replicators and the origin of life. J. Theor. Biol. 128, 463-483 (1987).
84. Szathmáry, E., Sandos, M. & Fernando, C. Evolutionary potential and requirements for minimal protocells. Top. Curr. Chem. 259, 167-211 (2005).
85. Takeuchi, N. & Hogeweg, P. Multilevel selection in models of prebiotic evolution II: a direct comparison of compartmentalization and spatial self-organization. PLoS Comput. Biol. 5, e1000542 (2009).
86. Konnyu, B. & Czaran, T. The evolution of enzyme specificity in the metabolic replicator model of prebiotic evolution. PLoS ONE 6, e20931 (2011).
87. Doudna, J. A., Couture, S. & Szostak, J. W. A multi-subunit ribozyme that is a catalyst of and template for complemtary strand RNA synthesis. Science 251, 1605-1608 (1991).
88. Ferris, J. P. Montmorillonite catalysis of 30-50 mer oligonucleotides: laboratory demonstration of potential steps in the origin of the RNA world. Orig. Life Evol. Biosph. 32, 311-332 (2002).
89. Lawless, J. G. & Yuen, G. U. Quantification of monocarboxylic acids in the Murchison carbonaceous meteorite. Nature 282, 396-398 (1979).
90. Deamer, D. W. The first living systems: a bioenergetics perspective. Microbiol. Mol. Biol. Rev. 61, 239-261 (1997).
91. Szostak, J. W., Bartel, D. P. & Luisi, P. L. Synthesizing life. Nature 409, 387-390 (2001).
92. Solé, R. V., Munteanu, A., Rodriguez-Caso, C. & Macía, J. Synthetic protocell biology: from reproduction to computation. Phil. Trans. Roy. Soc. B. 362, 1727-1739 (2007).
93. Chen, I. A, Roberts R. W, & Szostak J. W. The emergence of competition between model protocells. Science 305, 1474-1476 (2004).
94. Adamala, K. & Szostak, J. W. Competition between model protocells driven by an encapsulated catalyst. Nature Chem. 5, 495-501 (2013).
95. Strulson, C. A., Molden, R. C., Keating, C. D. & Bevilacqua, P. C. RNA catalysis through compartmentalization. Nature Chem. 4, 941-946 (2012).
96. Adamala, K. & Szostak, J. W. Nonenzymatic template-directed RNA synthesis inside model protocells. Science 342, 1098-1100 (2013).
97. Bansho, Y. et al. Importance of parasite RNA species repression for prolonged translation-coupled RNA self-replication. Chem. Biol. 19, 478-487 (2012).
98. Lehman, N. Evolution finds shelter in small spaces. Chem. Biol. 19, 439-440 (2012).
99. Ichihashi, N. et al. Darwinian evolution in a translation-coupled RNA replication system within a cell-like compartment. Nature Commun. 4, 2494 (2013).
100. von Kiedrowski, G., Otto, S. & Herdewijn, P. Welcome home, systems chemists! J. Syst. Chem. 1, 1 (2010).
101. Eschenmoser, A. Chemical etiology of nucleic acid structure. Science 284, 2118-2124 (1999).
102. Malyshev, D. A. et al. Solution structure, mechanism of replication, and optimization of an unnatural base pair. Chem. Eur. J. 16, 12650-12659 (2010).
103. Yang, Z., Chen, F., Alvarado, J. B. & Benner, S. A. Amplification, mutation, and sequencing of a six-letter synthetic genetic system. J. Am. Chem. Soc. 133, 15105-15112 (2011).
104. Kim, E.-K. & Switzer, C. Polymerase recognition of a Watson-Crick-like metal-mediated base pair: purine-2,6-dicarboxylatecopper(II)pyridine. ChemBioChem 14, 2403-2407 (2013).
105. Ebert, M. O., Mang, C., Krishnamurthy, R., Eschenmoser, A. & Jaun, B. The structure of a TNA-TNA complex in solution: NMR study of the octamer duplex derived from α-(l-threofuranosyl-)3′- 2′-CGAATTCG. J. Am. Chem. Soc. 130, 15105-15115 (2008).
106. Yang, Y.-W., Zhang, S., McCullum, E. O. & Chaput, J. C. Experimental evidence that GNA and TNA were not sequential polymers in the prebiotic evolution of RNA. J. Mol. Evol. 65, 289-295 (2007).
107. Yu, H., Zhang, S. & Chaput, J. C. Darwinian evolution of an alternative genetic system provides support for TNA as an RNA progenitor. Nature Chem.10, 183-187 (2012).
108. Pinheiro, V. B. et al. Synthetic genetic polymers capable of heredy and evolution. Science 336, 341-344 (2012).
109. Schlosser, K. & Li, Y. Biologically inspired synthetic enzymes made from DNA. Chem. Biol. 16, 315-322 (2009).
110. Silverman, S. K. DNA as a versatile chemical component for catalysis, encoding, and stereocontrol. Angew. Chem. Int. Ed. 49, 7180-7201 (2010).
111. Lazcano, A., Guerrero, R., Margulis, L. & Oro, J. The evolutionary transition from RNA to DNA in early cells. J. Mol. Evol. 27, 283-290 (1988).
112. Burton, A. S. & Lehman, N. DNA before proteins? Recent discoveries in nucleic acid catalysis strengthen the case. Astrobiology. 9, 125-130 (2009).
113. Ohtsuki, H. & Nowak, M. A. Prelife catalysts and replicators. Proc. Roy. Soc. B 276, 3783-3790 (2009).
114. Manapat, M. L., Chen, I. A. & Nowak, M. A. The basic reproductive ratio of life. J. Theor. Biol. 263, 317-327 (2010).
115. Chen, I. A. & Nowak. M. A. From prelife to life: how chemical kinetics become evolutionary dynamics. Acc. Chem. Res. 45, 2088-2096 (2012).
116. Wu, M. & Higgs, P. G. Origin of self-replicating biopolymers: autocatalytic feedback can jump-start the RNA world. J. Mol. Evol. 69, 541-554 (2009).
117. Wu, M. & Higgs, P. Comparison of the roles of momoner synthesis, polymerization, and recombination in the origin of autocatalytic sets of biopolymers. Astrobiology 11, 895-906 (2011).
118. Ma, W., Yu, C., Zhang, W. & Hu, J. A simple template-dependent ligase ribozyme as the RNA replicase emerging first in the RNA World. Astrobiology 10, 437-447 (2010).
119. Ma, W., Yu, C., Zhang, W. & Hu, J. Nucleotide synthetase ribozymes may have emerged first in the RNA World. RNA 13, 2012-2019 (2007).
120. Ma, W., Yu, C. & Zhang, W. Monte Carlo simulation of early molecular evolution in the RNA World. Biosystems 90, 28-39 (2007).