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      The progene hypothesis: the nucleoprotein world and how life began

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          Abstract

          Abstract

          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.

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          Dr. Thomas Dandekar, Dr. Bojan Zagrovic and Dr. Anthony Poole

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          Most cited references94

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          The origin of the genetic code.

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            Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions.

            At some stage in the origin of life, an informational polymer must have arisen by purely chemical means. According to one version of the 'RNA world' hypothesis this polymer was RNA, but attempts to provide experimental support for this have failed. In particular, although there has been some success demonstrating that 'activated' ribonucleotides can polymerize to form RNA, it is far from obvious how such ribonucleotides could have formed from their constituent parts (ribose and nucleobases). Ribose is difficult to form selectively, and the addition of nucleobases to ribose is inefficient in the case of purines and does not occur at all in the case of the canonical pyrimidines. Here we show that activated pyrimidine ribonucleotides can be formed in a short sequence that bypasses free ribose and the nucleobases, and instead proceeds through arabinose amino-oxazoline and anhydronucleoside intermediates. The starting materials for the synthesis-cyanamide, cyanoacetylene, glycolaldehyde, glyceraldehyde and inorganic phosphate-are plausible prebiotic feedstock molecules, and the conditions of the synthesis are consistent with potential early-Earth geochemical models. Although inorganic phosphate is only incorporated into the nucleotides at a late stage of the sequence, its presence from the start is essential as it controls three reactions in the earlier stages by acting as a general acid/base catalyst, a nucleophilic catalyst, a pH buffer and a chemical buffer. For prebiotic reaction sequences, our results highlight the importance of working with mixed chemical systems in which reactants for a particular reaction step can also control other steps.
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              Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena.

              In the macronuclear rRNA genes of Tetrahymena thermophila, a 413 bp intervening sequence (IVS) interrupts the 26S rRNA-coding region. A restriction fragment of the rDNA containing the IVS and portions of the adjacent rRNA sequences (exons) was inserted downstream from the lac UV5 promoter in a recombinant plasmid. Transcription of this template by purified Escherichia coli RNA polymerase in vitro produced a shortened version of the pre-rRNA, which was then deproteinized. When incubated with monovalent and divalent cations and a guanosine factor, this RNA underwent splicing. The reactions that were characterized included the precise excision of the IVS, attachment of guanosine to the 5' end of the IVS, covalent cyclization of the IVS and ligation of the exons. We conclude that splicing activity is intrinsic to the structure of the RNA, and that enzymes, small nuclear RNAs and folding of the pre-rRNA into an RNP are unnecessary for these reactions. We propose that the IVS portion of the RNA has several enzyme-like properties that enable it to break and reform phosphodiester bonds. The finding of autocatalytic rearrangements of RNA molecules has implications for the mechanism and the evolution of other reactions that involve RNA.
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                Author and article information

                Contributors
                altstein_anatoly@mail.ru
                Journal
                Biol Direct
                Biol. Direct
                Biology Direct
                BioMed Central (London )
                1745-6150
                26 November 2015
                26 November 2015
                2015
                : 10
                : 67
                Affiliations
                Institute of Gene Biology RAS, NF Gamaleya Federal Center of Epidemiology and Microbiology, IM Sechenov First Moscow State Medical University, Moscow, Russia
                Article
                96
                10.1186/s13062-015-0096-z
                4662029
                dcbfc538-fdfe-4836-879b-43c241fe8464
                © Altstein. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 12 July 2015
                : 13 November 2015
                Categories
                Review
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                © The Author(s) 2015

                Life sciences
                origin of life,first genetic system,progene,origin of replication and translation,genetic code,selection of organic compounds

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