Formation of nucleobases in a Miller–Urey reducing atmosphere

Abstract

The Miller-Urey experiments pioneered modern research on the molecular origins of life, but their actual relevance in this field was later questioned because the gas mixture used in their research is considered too reducing with respect to the most accepted hypotheses for the conditions on primordial Earth. In particular, the production of only amino acids has been taken as evidence of the limited relevance of the results. Here, we report an experimental work, combined with state-of-the-art computational methods, in which both electric discharge and laser-driven plasma impact simulations were carried out in a reducing atmosphere containing NH 3 + CO. We show that RNA nucleobases are synthesized in these experiments, strongly supporting the possibility of the emergence of biologically relevant molecules in a reducing atmosphere. The reconstructed synthetic pathways indicate that small radicals and formamide play a crucial role, in agreement with a number of recent experimental and theoretical results. The following explorations showed that a broad array of amino acids could be synthesized, but there was no evidence that all of the fundamental molecules of the RNA genetic code could be produced alongside others in this type of experiment (2-5). Additionally, the significant persistence of reducing atmospheres in a geological timescale has been seriously debated (6). Finally, many scientists have claimed that this experiment is not related to early-Earth conditions and does not provide fundamental building blocks (i.e., nucleobases) important for the evolution of early life possibly based on RNA (7-13). In 2001, Saladino, Di Mauro, and coworkers (14) proposed that the parent molecule for the one-pot synthesis of nucleobases is formamide (15-23). Their team, together with other authors, demonstrated the formation of (not only) fundamental nucleobases for the origin of RNA in experiments involving the heating of formamide in presence of manifold catalysts (17,(24)(25)(26), upon UV irradiation (27), proton (28) and heavy-particle radiation (29), exposition to shock waves (18), etc. Recently, Hörst et al. (30) also referred to a positive result on qualitative detection of RNA nucleobases and manifold amino acids from tholines created in a N 2 , CH 4 , CO mixture. Their experiment simulated the atmosphere of Titan upon electric discharge. Such experimental results as well as theoretical expectations (31) show that reduced, relatively reactive atmospheres are likely to be more efficient for the synthesis of biomolecules (32). However, it should be noted that several papers report also the formation of biomolecules under neutral (N 2 , CO 2 , H 2 O) conditions (33-35). In our study, we found an interconnection between the original ideas of the pioneering Miller-Urey studies devoted to prebiotic synthesis in a reducing atmosphere and recent results identifying the chemistry of formamide as a source for the synthesis of nucleobases. In addition to traditional hydrogen cyanide (HCN)-based or reducing atmosphere-based concept...

HNCO-based synthesis of formamide in planetary atmospheres

“…Formamide-based chemistry is a broadly discussed scenario relating to the origin of biomolecules (Saladino et al 2004(Saladino et al , 2012bFerus et al 2011bFerus et al , 2012Ferus et al , 2014Ferus et al , 2017bSaitta & Saija 2014;Pino et al 2015;Šponer et al 2016a,b;Adam et al 2018;Becker et al 2018;Benner et al 2012). Besides the traditional HCNand reducing-atmospheres based biomolecules synthesis (Ferris et al 1974;Yuasa et al 1984;Levy et al 1999;Sutherland 2016;Civiš et al 2017), the current evidence shows that the formamide molecule did not necessary play role of merely starting parent prebiotic precursor, but also it could serve as an intermediate compound in prebiotic synthesis (Ferus et al 2017b).…”

“…Besides the traditional HCNand reducing-atmospheres based biomolecules synthesis (Ferris et al 1974;Yuasa et al 1984;Levy et al 1999;Sutherland 2016;Civiš et al 2017), the current evidence shows that the formamide molecule did not necessary play role of merely starting parent prebiotic precursor, but also it could serve as an intermediate compound in prebiotic synthesis (Ferus et al 2017b). In fact, it has been demonstrated that it acted either as substrate or as intermediate in a series of complex reactions starting from very reactive small radicals and leading to a broad palette of biomolecules, for example, all the canonical nucleobases of the genetic code, ribose and other sugars, amino acids or even fatty acids (Saladino et al 2011(Saladino et al , 2015Ferus et al 2015b).…”

“…The former variable represents the progress along the chemical transformation (i.e., the geometrical evolution of the system from the reactants toward the products) whereas the latter the distance from an ideal pathway. product of the above-mentioned reaction) is expected to decrease with respect to that of the simpler reactants mainly because of entropic reasons (Ferus et al 2017b). It has recently been shown, indeed, that under those conditions, formamide can be exploited as a key intermediate and parent compound of the synthesis of RNA nucleobases (Ferus et al 2017b).…”

“…During the last decade, various chemical processes depending on the physical and chemical conditions encountered in several astrophysical environments have been discussed as possible sources of the formamide species, such as, for example, HCN hydrolysis (Saladino et al 2012b;Bada et al 2016;Šponer et al 2016b), ammonium-formate dehydration (Šponer et al 2016a) or direct synthesis from CO and NH 3 atmosphere (Ferus et al 2017b). In many cases, however, the proposed formation pathways are poorly constrained both experimentally and theoretically (Taquet et al 2015).…”

Non-Watson–Crick RNA synthesis suited to origin functions

“…Though guanine is less abundantly made, it can occur in the same order of concentration as adenine (Borquez et al 2005). Other possible nucleobase sources such as impact on a reducing atmosphere also supply the synthetic impetus for both standard purines (Ferus et al 2017). Most relevantly, adenine and guanine of extraterrestrial origin occur together in multiple carbonaceous chondrite meteorites (Callahan et al 2011).…”