The progene hypothesis: the nucleoprotein world and how life began
Open accessAbstract
In this article, I review the results of studies on the origin of life distinct from the popular RNA world hypothesis. The alternate scenario postulates the origin of the first bimolecular genetic system (a polynucleotide gene and a polypeptide processive polymerase) with simultaneous replication and translation and includes the following key features: 1. The bimolecular genetic system emerges not from mononucleotides and monoamino acids, but from progenes, namely, trinucleotides aminoacylated on 3'-end by a non-random amino acid (NpNpNp ~ pX ~ Aa, where N--deoxyribo- or ribonucleoside, p--phosphate, X--a bifunctional agent, for example ribose, Aa--amino acid, ~ macroerge bond). Progenes are used as substrates for simultaneous synthesis of a polynucleotide and a polypeptide. Growth of the system is controlled by the growing polypeptide, and the bimolecular genetic system emerges as an extremely rare event. The first living being (virus-like organism protoviroid, Protoviroidum primum) arises and reproduces in prebiotic liposome-like structures using progenes. A population of protoviroids possessing the genetic system evolves in accordance with the Darwinian principle. Early evolution from protoviroid world to protocell world is shortly described. 2. The progene forming mechanism (NpNp + Np ~ pX ~ Aa) makes it possible to explain the emergence of the prebiotic physicochemical group genetic code, as well as the selection of organic compounds for the future genetic system from the racemic environment. 3. The protoviroid is reproduced on a progene basis via replicative transcription-translation (RTT, the first molecular genetic process) that is similar to its modern counterparts. Nothing is required for the emergence and reproduction of the protoviroid except for progenes and conditions for their formation. 4. The general scheme of early evolution is as follows: prebiotic world → protoviroid (nucleoprotein) world → protocell (DNA-RNA-protein) world → LUCA (Last Universal Common Ancestor) → modern cell world. This scheme exclude the existence of an independent RNA world as predecessor of the cellular world.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The genetic code evolved as pathways for the synthesis of new amino acids became available.
“Therefore, the genetic code evolved as pathways for the synthesis of new amino acids became available [73,92,102].”
From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [92]
In “Consequence 3. The molecular mechanism of genetic code arising” (page not specified), the paper proposes that the primary genetic code arose when only a limited set of amino acids was abundant and several others were scarce or absent. This supports a changing amino-acid repertoire, but the passages do not say that the code evolved as pathways for synthesizing new amino acids became available. (LLM, conf=0.78)
Experimental — accuracy not yet measuredThe assembly of large and small subunits is dependent upon ribosomal proteins.
“The assembly of large and small subunits that are dependent upon ribosomal proteins [17,92].”
From The Origin of Prebiotic Information System in the Peptide/RNA World: A Simulation Model of the Evolution of Translation and the Genetic Code (2019) · cites this paper as [92]
The Background and general approach discusses ribosomal RNA activity, and the reviewer’s comments say ribosomes cannot move along a template without their protein parts. Neither passage addresses whether assembly of the large and small ribosomal subunits depends on ribosomal proteins. Searches for subunit assembly and protein dependence found no passage that settles the claim. (LLM, conf=0.72)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Before enzymes and templates: theory of surface metabolism
Wächtershäuser, G. (1988) · Microbiological Reviews · doi:10.1128/mmbr.52.4.452-484.1988 · Cited by 1,242 · see citing works
RNA-catalyzed RNA polymerization: Accurate and general RNA-templated primer extension.
Johnston, W. K., Unrau, P. J., Lawrence, M. S., Glasner, M. E., & Bartel, D. P. (2001) · Science · doi:10.1126/science.1060786 · Cited by 768 · see citing works
Carbonaceous Meteorites Contain a Wide Range of Extraterrestrial Nucleobases
Callahan, M. P., Smith, K. E., Cleaves, H. J., Ruzicka, J., Stern, J. C., Glavin, D. P., House, C. H., & Dworkin, J. P. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106493108 · Cited by 590 · see citing works
Chiral selection in poly(C)-directed synthesis of oligo(G)
Joyce, G. F., Visser, G. M., van Boeckel, C. A. A., van Boom, J. H., Orgel, L. E., & van Westrenen, J. (1984) · Nature · doi:10.1038/310602a0 · Cited by 398 · see citing works
Origin and evolution of the genetic code: The universal enigma
Koonin, E. V., & Novozhilov, A. S. (2009) · IUBMB Life · doi:10.1002/iub.146 · Cited by 392 · see citing works
RNA, the first macromolecular catalyst: the ribosome is a ribozyme
Steitz, T. A., & Moore, P. B. (2003) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(03)00169-5 · Cited by 319 · see citing works
Prebiotic Synthesis of Simple Sugars by Photoredox Systems Chemistry
Ritson, D., & Sutherland, J. D. (2012) · Nature Chemistry · doi:10.1038/nchem.1467 · Cited by 258 · see citing works
A kinetic study of the growth of fatty acid vesicles
Chen, I. A., & Szostak, J. W. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.039875 · Cited by 251 · see citing works
Wolf, Y. I., & Koonin, E. V. (2007) · Biology Direct · doi:10.1186/1745-6150-2-14 · Cited by 235 · cited 1× · see citing works
“Evolution of translation is the main way of transition to the modern cells [37, 40, 97].”
BackgroundRNA–Amino Acid Binding: A Stereochemical Era for the Genetic Code
Yarus, M., Widmann, J. J., & Knight, R. (2009) · Journal of Molecular Evolution · doi:10.1007/s00239-009-9270-1 · Cited by 198 · see citing works
Non-enzymatic template-directed synthesis on RNA random copolymers
Joyce, G. F., Inoue, T., & Orgel, L. E. (1984) · Journal of Molecular Biology · doi:10.1016/0022-2836(84)90425-x · Cited by 178 · see citing works
What RNA World? Why a Peptide/RNA Partnership Merits Renewed Experimental Attention
Carter, C. (2015) · Life · doi:10.3390/life5010294 · Cited by 95 · see citing works
The emergence of life on Earth
Lahav, N., Nir, S., & Elitzur, A. C. (2001) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(01)00003-7 · Cited by 73 · see citing works
First Life: Discovering the Connections between Stars, Cells, and How Life Began
Deamer, D. (2011) · doi:10.1525/9780520948952 · Cited by 66 · see citing works
Prebiotic co-evolution of self-replication and translation or RNA world?
Lahav, N. (1991) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(05)80368-6 · Cited by 28 · see citing works
Flagged first, then by citations
Research works printed but not linked: 67
- [3]Miller S A production of amino acids under possible primitive earth conditions Science 1953 117 528 9 10.1126/science.117.3046.528 13056598 · DOI · Paper page
- [6]Powner MW Gerland B John D Sutherland JD Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions Nature 2009 459 239 242 10.1038/nature08013 19444213 · DOI · Paper page
- [7]Patel BH Percivalle C Ritson DJ Duffy CD Sutherland JD Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism Nat Chem 2015 7 4 301 7 10.1038/nchem.2202 25803468 PMC4568310 · DOI · Paper page
- [8]Biron JP Parkes AL Pascal R Sutherland JD Expeditious, potentially primordial, aminoacylation of nucleotides Angew Chem Int Ed Engl 2005 44 41 6731 4 10.1002/anie.200501591 16187390 · DOI
- [9]Rauchfuss H Chemical evolution and the origin of life 2008 Berlin Springer
- [11]Dyson F Origin of life 1985 Cambridge Cambridge University Press
- [12]Crick FH The origin of the genetic code J Mol Biol 1968 38 367 379 10.1016/0022-2836(68)90392-6 4887876 · DOI · Paper page
- [13]Orgel L Evolution of the genetic apparatus J Mol Biol 1968 38 3 381 393 10.1016/0022-2836(68)90393-8 5718557 · DOI · Paper page
- [14]Inoe T Orgel L A nonenzymatic polymerase RNA model Science 1983 219 859 862 10.1126/science.6186026 6186026 · DOI · Paper page
- [15]Kruger K Grabowski PJ Zaug AJ Sands J Gottschling DE Cech TR Self-splicing RNA: Autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena Cell 1982 31 147 157 10.1016/0092-8674(82)90414-7 6297745 · DOI · Paper page
- [16]Guerrier-Takada C Gardiner K Marsh T Pace N Altman S The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme Cell 1983 35 849 857 10.1016/0092-8674(83)90117-4 6197186 · DOI · Paper page
- [17]Gilbert W The RNA World Nat 1986 319 618 10.1038/319618a0 · DOI · Paper page
- [18]Cech TR A model for the RNA-catalyzed replication of RNA Proc Natl Acad Sci U S A 1986 12 4360 3 10.1073/pnas.83.12.4360 2424025 PMC323732 · DOI
- [19]Sharp PA Eisenberg D The evolution of catalytic function Science 1987 238 4228 729 730 10.1126/science.2445035 2445035 · DOI
- [20]Bernhardt HS The RNA, world hypothesis: the worst theory of the early evolution of life (except for all the others) Biol Direct 2012 7 13 10.1186/1745-6150-7-13 22793875 PMC3495036 · DOI
- [21]Beaudry AA Joyce GF Directed evolution of an RNA enzyme Science 1992 257 635 41 10.1126/science.1496376 1496376 · DOI
- [22]Green R Szostak JW Selection of a ribozyme that functions as a superior template in a self-copying reaction Science 1992 258 5090 1910 5 10.1126/science.1470913 1470913 · DOI
- [23]Suga H Futai K Jin K Metal ion requirements in artificial ribozymes that catalyze aminoacylation and redox reactions Met Ions Life Sci 2011 9 277 97 10.1039/9781849732512-00277 22010276 · DOI
- [24]Wilson DS Szostak JW In vitro selection of functional nucleic acids Annu Rev Biochem 1999 68 611 47 10.1146/annurev.biochem.68.1.611 10872462 · DOI
- [25]Seelig B Szostak JW (2007) Selection and evolution of enzymes from a partially randomized non-catalytic scaffold Nature 2007 448 828 31 10.1038/nature06032 17700701 PMC4476047 · DOI
- [27]McGinness KE Joyce GF In search of an RNA replicase ribozyme Chem Biol 2003 10 1 5 14 10.1016/S1074-5521(03)00003-6 12573693 · DOI
- [28]Attwater J Wochner A Holliger P In-ice evolution of RNA polymerase ribozyme activity Nat Chem 2013 5 12 1011 8 10.1038/nchem.1781 24256864 PMC3920166 · DOI · Paper page
- [29]Cuenoud B Szostak JW A DNA metalloenzyme with DNA ligase activity Nature 1995 375 6532 611 4 10.1038/375611a0 7791880 · DOI
- [32]Joyce GF RNA evolution and the origins of life Nature 1989 338 217 224 10.1038/338217a0 2466202 · DOI · Paper page
- [33]Robertson MP Joyce GF The origin of the RNA world Cold Sping Harbor Perspect Biol 2012 4 5 PMC3331698 20739415
- [34]Schwartz AW Speculation on the RNA precursor problem J Theor Biol 1997 187 4 523 7 10.1006/jtbi.1996.0386 9299296 · DOI
- [35]Dworkin JP Lazcano A Miller SL The roads to and from the RNA world J Theor Biol 2003 222 1 127 34 10.1016/S0022-5193(03)00020-1 12699739 · DOI
- [36]Lazcano A Miller SL the origin and early evolution of life: prebiotic chemistry, the pre- RNA world, and time Cell 1996 85 6 793 8 10.1016/S0092-8674(00)81263-5 8681375 · DOI
- [37]Poole AM Jeffares DC Penny D The path from DNA world J Mol Evol 1998 46 1 1 17 10.1007/PL00006275 9419221 · DOI · Paper page
- [38]Takeuchi N Hogeweg P Koonin EV On the origin of DNA genomes: evolution of the division of labor between template and catalyst in model replicator systems PLoS Comput Biol 2011 7 3 e1002024 10.1371/journal.pcbi.1002024 21455287 PMC3063752 · DOI
- [41]Frances BR Hypothesis that the genetic code originated in couple synthesis of proteins and the evolutionary predecessors of nucleic acids in primitive cells Life 2015 5 1 467 505 10.3390/life5010467 25679748 PMC4390864 · DOI
- [42]Bowman JC Hud NV Williams LD The ribosome challenge to the RNA world J Mol Evol 2015 80 3–4 143 61 10.1007/s00239-015-9669-9 25739364 · DOI · Paper page
- [43]Caetano-Anollés G Ancestral insertions and expansions of rRNA do not support an origin of the ribosome in its Peptidyl transferase center J Mol Evol 2015 80 3–4 162 5 10.1007/s00239-015-9677-9 25864085 PMC4555209 · DOI
- [44]Eigen M Schuster P The hypercycle. A principle of natural self-organization. Part a: emergence of the hypercycle Naturwissenschaften 1977 64 11 541 565 10.1007/BF00450633 593400 · DOI · Paper page
- [50]Al’tshtein AD Efimov AV Physicochemical basis of origin of the genetic code: stereochemical analysis of interaction of amino acid and nucleotides on the basis of the progene hypothesis Mol Biol 1988 22 1411 1429 3221859
- [53]Altstein AD The origin of protocells Orig Life Evol Biosph 1996 26 3–5 477 8 10.1007/BF02459879 · DOI
- [58]Folsome CE Morowitz HJ Prebiological membranes: synthesis and properties Space Life Sci 1969 1 4 538 44 5406452
- [59]Morowitz HJ Heinz B Deamer DW The chemical logic of a minimum protocell Orig Life Evol Biosph 1988 18 3 281 7 10.1007/BF01804674 3226720 · DOI · Paper page
- [60]Hargreaves WR Deamer DW Liposomes from ionic, single-chain amphiphiles Biochemistry 1978 17 18 3759 68 10.1021/bi00611a014 698196 · DOI
- [61]Deamer DW Barchfeld GL Encapsulation of macromolecules by lipid vesicles under simulated prebiotic conditions J Mol Evol 1982 18 3 203 6 10.1007/BF01733047 7097780 · DOI · Paper page
- [62]Monnard PA Luptak A Deamer DW Models of primitive cellular life: polymerases and templates in liposomes Philos Trans R Soc Lond B Biol Sci 2007 362 1486 1741 50 10.1098/rstb.2007.2066 17472931 PMC2442390 · DOI
- [63]Zhu TF Szostak JW Preparation of large monodisperse vesicles PLoS One 2009 4 4 e5009 10.1371/journal.pone.0005009 19347043 PMC2661144 · DOI
- [64]Zhu TF Szostak JW Coupled growth and division of model protocell membranes J Am Chem Soc 2009 131 15 5705 13 10.1021/ja900919c 19323552 PMC2669828 · DOI · Paper page
- [68]Dolinnaya NG Sokolova NI Gryaznova OI Shabarova ZA Site-directed modification of DNA duplexes by chemical ligation Nucleic Acids Res 1988 16 9 3721 3738 10.1093/nar/16.9.3721 3375071 PMC336552 · DOI
- [69]Sulston J Lohrmann R Orgel LE Schneider-Bernloehr H Weimann BJ Miles HT Non-enzymic oligonucleotide synthesis on a polycytidylate template J Mol Biol 1969 40 2 227 34 10.1016/0022-2836(69)90471-9 5365010 · DOI
- [70]Lohrmann R Orgel LE Template-directed synthesis of high molecular weight polynucleotide analogues Nature 1976 261 5558 342 4 10.1038/261342a0 1272416 · DOI
- [72]Nelsestuen GL Amino acid-directed nucleic acid synthesis. A possible mechanism in the origin of life J Mol Evol 1978 11 2 109 20 10.1007/BF01733887 671559 · DOI
- [73]Zielinski WS Orgel LE The template properties of tetranucleoside triphosphoramidates having cytosine-guanosine residues J Mol Evol 1989 29 4 281 3 10.1007/BF02103614 2514268 · DOI
- [75]Kirnos MD Khudyakov IY Alexandrushkina NI Vanyushin BF 2-aminoadenine is an adenine substituting for a base in S-2 L cyanophage DNA Nature 1977 270 5635 369 70 10.1038/270369a0 413053 · DOI
- [76]Weber A Pizzarello S The peptide-catalyzed stereospecific synthesis of tetroses: a possible model for prebiotic molecular evolution Proc Natl Acad Sci U S A 2006 103 12713 12717 10.1073/pnas.0602320103 16905650 PMC1568914 · DOI
- [77]Breslow R Cheng ZL L-amino acids catalyze the formation of an excess of D-glyceraldehyde, and thus of other D sugars, under credible prebiotic conditions Proc Natl Acad Sci U S A 2010 107 13 5723 5 10.1073/pnas.1001639107 20231487 PMC2851924 · DOI · Paper page
- [80]Szathmáry E The origin of the genetic code: amino acids as cofactors in an RNA world Trends Genet 1999 15 6 223 9 10.1016/S0168-9525(99)01730-8 10354582 · DOI · Paper page
- [81]Hajnic M Osorio JI Zagrovic B Interaction preferences between nucleobase mimetics and amino acids in aqueous solutions Phys Chem Chem Phys 2015 17 33 21414 22 10.1039/C5CP01486G 26219945 · DOI
- [82]Hlevnjak M Zagrovic B Malleable nature of mRNA-protein compositional complementarity and its functional significance Nucleic Acids Res 2015 43 6 3012 21 10.1093/nar/gkv166 25753660 PMC4381073 · DOI
- [83]de Ruiter A Zagrovic B Absolute binding-free energies between standard RNA/DNA nucleobases and amino-acid sidechain analogs in different environments Nucleic Acids Res 2015 43 2 708 18 10.1093/nar/gku1344 25550435 PMC4333394 · DOI
- [84]Weber AL Miller SL Reasons for the occurrence of the twenty coded protein amino acids J Mol Evol 1981 17 273 284 10.1007/BF01795749 7277510 · DOI
- [85]Higgs PG Pudritz RE A thermodynamic basis for prebiotic amino acid synthesis and the nature of the first genetic code Astrobiology 2009 9 5 483 90 10.1089/ast.2008.0280 19566427 · DOI · Paper page
- [86]Calvin M Chemical evolution. Molecular evolution towards the origin of living systems on the Earth and elsewhere 1969 Oxford Clarendon
- [91]Wächtershäuser G On the chemistry and evolution of the pioneer organism Chem Biodivers 2007 4 4 584 602 10.1002/cbdv.200790052 17443873 · DOI
- [92]Huber C Eisenreich W Hecht S Wächtershäuser G A possible primordial peptide cycle Science 2003 301 5635 938 40 10.1126/science.1086501 12920291 · DOI
- [93]Baross JA Hoffman SA Submarine hydrothermal vents and associated gradient environmets as site of origin and evolution of life Orig Life 1985 15 327 345 10.1007/BF01808177 · DOI · Paper page
- [94]Russell MJ Hall AJ The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front J Geol Soc London 1997 154 3 377 402 10.1144/gsjgs.154.3.0377 11541234 · DOI · Paper page
- [95]Martin W Russell MJ On the origin of biochemistry at an alkaline hydrothermal vent Philos Trans R Soc Lond B Biol Sci 2007 362 1486 1887 925 10.1098/rstb.2006.1881 17255002 PMC2442388 · DOI · Paper page
- [96]Griffiths G Cell evolution and the problem of membrane topology Nat Rev Mol Cell Biol 2007 8 12 1018 24 10.1038/nrm2287 17971839 · DOI
- [97]Koonin EV The logic of chance. Nature and origin of biologic evolution 2011 Upper Saddle River Pearson Education, Inc
- [98]Ohno S Evolution by gene duplication 1971 Berlin Springer Verlag
- [99]Orgel LE Gene-duplication and the origin of proteins with novel functions J Theor Biol 1977 67 4 773 10.1016/0022-5193(77)90262-4 904347 · DOI
Cited by
Sorted by citations
Chatterjee, S., & Yadav, S. (2019) · Life · doi:10.3390/life9010025 · Cited by 80 · see citing works
“The assembly of large and small subunits that are dependent upon ribosomal proteins [17,92].”
Kunnev, D., & Gospodinov, A. (2018) · Life · doi:10.3390/life8040044 · Cited by 24 · see citing works
- Authors
- Altstein, A. D.
- Affiliations
- Sechenov University (RU)
- Corresponding author
- Altstein, Anatoly D.
- Venue
- Biology Direct
- Published
- 2015-11-26
- Volume
- 10
- Issue
- 1
- Pages
- 67-67
- ISSN
- 1745-6150 (ISSN-L)
- PMC
- PMC4662029
- OpenAlex
- W2178515564
- Cited by
- 20
- References
- 15
- Citations by year
- 2026: 4 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 1 · 2020: 1 · 2019: 3 · 2018: 3
- FWCI
- 0.08
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Biology Direct (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- origin of life, protocells, origin of the genetic code, early evolution, last universal common ancestor, aminoacylation
- MeSH terms
- Origin of Life, Genetic Code, Models, Genetic, Nucleoproteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review