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Prebiotic Chemistry Themed Issue View Online / Journal Homepage / Table of Contents for this issue This article was published as part of the Prebiotic chemistry themed issue Guest editors Jean-François Lambert, Mariona Sodupe and Piero Ugliengo Please take a look at the issue 16 2012 table of contents to access other reviews in this themed issue Downloaded by University of Oxford on 26 July 2012 Published on 08 June 2012 http://pubs.rsc.org | doi:10.1039/C2CS35066A View Online Chem Soc Rev Dynamic Article Links Cite this: Chem. Soc. Rev., 2012, 41, 5526–5565 www.rsc.org/csr CRITICAL REVIEW Genetics first or metabolism first? The formamide cluew Raffaele Saladino,*a Giorgia Botta,a Samanta Pino,b Giovanna Costanzoc and Ernesto Di Mauro*d Received 6th March 2012 DOI: 10.1039/c2cs35066a Life is made of the intimate interaction of metabolism and genetics, both built around the chemistry of the most common elements of the Universe (hydrogen, oxygen, nitrogen, and carbon). The transmissible interaction of metabolic and genetic cycles results in the hypercycles of organization and de-organization of chemical information, of living and non-living. The origin-of-life quest has long been split into several attitudes exemplified by the aphorisms ‘‘genetics-first’’ or ‘‘metabolism-first’’. Recently, the opposition between these approaches has been solved by more unitary theoretical and experimental frames taking into account energetic, evolutionary, proto-metabolic and environmental aspects. Nevertheless, a unitary and simple chemical frame is still needed that could afford both the precursors of the synthetic pathways eventually leading to RNA and to the key components of the central metabolic cycles, possibly connected with the synthesis of fatty acids. In order to approach the problem of the origin of life it is therefore reasonable to start from the assumption that both metabolism and genetics had a common origin, shared a common chemical frame, and were embedded under physical–chemical conditions favourable for the onset of both. The singleness of such a prebiotically productive chemical process would partake of Darwinian advantages over more complex fragmentary Downloaded by University of Oxford on 26 July 2012 chemical systems. The prebiotic chemistry of formamide affords in a single and simple Published on 08 June 2012 http://pubs.rsc.org | doi:10.1039/C2CS35066A physical–chemical frame nucleic bases, acyclonucleosides, nucleotides, biogenic carboxylic acids, sugars, amino sugars, amino acids and condensing agents. Thus, we suggest the possibility that formamide could have jointly provided the main components for the onset of both (pre)genetic and (pre)metabolic processes. As a note of caution, we discuss the fact that these observations only indicate possible solutions at the level of organic substrates, not at the systemic chemical level. 1. Introduction the task is paramount. This endeavour necessarily passes through the untangling of the riddles specific to each type of It is a shared opinion that we will never know exactly how life biomolecules (nucleic acids, proteins, lipids, precursors of started on this planet but that at one point it will be possible to energy metabolisms) and to their initial, possibly cooperative reconstruct the likely chemical frames into which the different interactions. Before even considering the kick-starting events prebiotic processes organized themselves. Understanding the leading to the onset of cycles, the relevant prebiotically fertile key passages leading to their reciprocal interactions will follow. chemical frame(s) must be identified. Or was it rather a multifaceted single frame? The complexity of Building on the rationale illuminatingly defined by Victor Oparin,1 the last six decades have witnessed solid and con- a Dipartimento di Agrobiologia ed Agrochimica, tinuous progress, starting from the seminal Stanley Miller’s Universita` della Tuscia, Via San Camillo De Lellis, 01100 Viterbo, discoveries,2 reviewed in ref. 3. We will here examine ground- Italy. E-mail: [email protected] b Dipartimento di Biologia e Biotecnologie ‘‘Charles Darwin’’, breaking and recent observations related to the formation of ‘‘Sapienza’’ Universita` di Roma, P.leAldo Moro, 5, Rome 00185, the precursors of biomolecules, keeping in mind that an Italy. E-mail: [email protected] exhaustive analysis of this topic is impossible in a single article c Istituto di Biologia e e Patologia Molecolari, CNR, P.le Aldo Moro, 5, Rome 00185, Italy. E-mail: [email protected] and that restrictive choices need to be a priori made. Thus, we 4,5 d Istituto Pasteur ‘‘Fondazione Cenci-Bolognetti’’ c/o Dipartimento di reasoned following a Bayesian inference approach, consisting Biologia e Biotecnologie ‘‘Charles Darwin’’, ‘‘Sapienza’’ Universita` of changing our subjective degree of belief rationally in order di Roma, P.leAldo Moro, 5, Rome 00185, Italy. to account for evidence. When no decision is possible, we E-mail: [email protected]; Fax: +39 064440812; Tel: +39 0649912880 appealed to Occam’s lex parsimoniae, usually phrased: simpler w Part of the prebiotic chemistry themed issue. explanations are, other things being equal, generally better 5526 Chem. Soc. Rev., 2012, 41, 5526–5565 This journal is c The Royal Society of Chemistry 2012 View Online than more complex ones. As restated by Bertrand Russel: applies to the possible initial cooperation between vesicles ‘‘whenever possible, substitute constructions out of known and RNA,7 and to the relationships among the key compo- entities for inferences to unknown entities’’.6 nents of metabolic cycles. As suggested by Vijayasarathy and The available evidence bayesianally leads to hydrogen Harold J. Morowitz,8 the first set of prebiotic processes cyanide (HCN) chemistry and, inside its frame of reference, reasonably consisted of a small group of organic reactions, to formamide (NH2CHO) chemistry. The two frames are including the 11 key chemical transformations in the core of not in conflict (as will be discussed) but, rather, the second autotrophic anabolism: hydrolysis/dehydration, carboxylation/ is a chapter of the first. However, the specific attributes decarboxylation, oxidation/reduction, phosphorylation/ of stability, reactivity and the chemical properties of forma- dephosphorylation, isomerization, transamination and transfer mide make it a preferential starting point for prebiotic of functional groups. synthetic processes. We will present evidence pointing to Were these compounds present in the same ‘‘warm little the possible role of formamide-plus-minerals in the syntheses pond’’?9 A brief review of the principal models dealing with of a large part of the relevant starting components in pre- the onset of metabolisms will allow us to point to evidence biotic scenarios, namely nucleic acid components, amino related to a possible formamide-based unitary chemical frame acids, sugars, amino sugars and carboxylic acids. The connec- for metabolism and genetics. Thus, possible passages from the tion of formamide with all these compounds is presented in compounds afforded by formamide to higher complexity Fig. 1. organization levels will be indicated, particular attention being In Occamian terms, if polymerization of ribopolymers had devoted to the spontaneous generation of RNA, to the to occur, all the necessary components had to be present in the problem of the onset of metabolic cycles and to their possible same environment at the same time. A similar reasoning coexistence in the same chemical scenario. Raffaele Saladino was born in Giorgia Botta was born in Rome in 1964. He obtained a Fredericton, Canada in 1979. Masters degree in Chemistry She received a Masters degree at University ‘‘Sapienza’’, Rome, in Medicinal Chemistry at the in 1989 and a PhD in Chemical University of Siena (Italy) in Sciences at the same University 2005 and a PhD in Medicinal in 1993. After post-doctoral Chemistry from the same Downloaded by University of Oxford on 26 July 2012 training at the University University in 2008. Since of Montreal (Canada) and October 2010 she has been Published on 08 June 2012 http://pubs.rsc.org | doi:10.1039/C2CS35066A teaching and research posi- working as a Postdoctoral tions at the University of Research Associate at the Tuscia, Viterbo, Italy he is University of Viterbo (Italy) now an Associate Professor of in collaboration with Prof. Organic & Bioorganic Chemistry Raffaele Saladino. Her Raffaele Saladino at the same University. He is Giorgia Botta research interests are in the involved in studies on prebiotic field of Organic, Analytical chemistry, green catalysis and oxidative transformations of and Medicinal Chemistry with particular interest in the Synthesis natural substances mainly focused on bioactive compounds. of novel Antiviral and Anticancer agents and in the field of Astrobiology with particular interest in the Origin of Life. Samanta Pino was born in Giovanna Maria Costanzo Priverno, Italy in 1978. She was born in Rome, Italy, in studied Biology at the Roma 1962. She obtained her Degree Tre, University of Rome. She in Biological Sciences from received her PhD in Pasteurian ‘‘Sapienza’’ University of Sciences at the Department Rome, Italy, in 1987. In 1991 of Genetics and Molecular she joined the Dept. of Bio- Biology, University of Rome chemistry and Cell Biology ‘‘Sapienza’’ in 2009, working in at the University of New York the field of prebiotic chemistry. at Stony Brook (USA) as a Her primary research interests postdoctoral fellow. Since are currently focused on the 2001 she
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