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Emergence of Homochirality in Large Molecular Systems Gabin Laurent, David Lacoste, Pierre Gaspard

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Emergence of Homochirality in Large Molecular Systems Gabin Laurent, David Lacoste, Pierre Gaspard Emergence of homochirality in large molecular systems Gabin Laurent, David Lacoste, Pierre Gaspard To cite this version: Gabin Laurent, David Lacoste, Pierre Gaspard. Emergence of homochirality in large molecular sys- tems. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2021, 118 (3), pp.e2012741118. 10.1073/pnas.2012741118. hal-03117080 HAL Id: hal-03117080 https://hal.archives-ouvertes.fr/hal-03117080 Submitted on 21 Jan 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Emergence of homochirality in large molecular systems Gabin Laurenta,1, David Lacostea, and Pierre Gaspardb aGulliver, UMR CNRS 7083, Ecole´ Sup´erieure de Physique et de Chimie Industrielles de la Ville de Paris, Paris Sciences et Lettres Research university, F-75231 Paris, France bCenter for Nonlinear Phenomena and Complex Systems, Universit´eLibre de Bruxelles, B-1050 Brussels, Blegium. [email protected] Abstract The selection of a single molecular handedness, or homochirality across all living matter, is a mystery in the origin of life. Frank's seminal model showed in the fifties how chiral symmetry breaking can occur in non-equilibrium chemical networks. However, an important shortcoming in this classic model is that it considers a small number of species, while there is no reason for the prebiotic system, in which homochirality first appeared, to have had such a simple composition. Furthermore, this model does not provide information on what could have been the size of the molecules involved in this homochiral prebiotic system. Here, we show that large molecular systems are likely to undergo a phase transition towards a homochiral state, as a consequence of the fact that they contain a large number of chiral species. Using chemoinformatics tools, we quantify how abundant are chiral species in the chemical universe of all possible molecules of a given length. Then, we propose that Frank's model should be extended to include a large number of species, in order to possess the transition towards homochirality as confirmed by numerical simulations. Finally, using random matrix theory, we prove that large non-equilibrium reaction networks possess a generic and robust phase transition towards a homochiral state. Keywords: homochirality, origin of life, prebiotic chemistry, random matrices, statistical physics Life on Earth relies on chiral molecules that is, species servation [4{15]. not superposable on their mirror images.− A given biolog- ical molecule forms with its mirror image a pair of enan- tiomers. Homochirality precisely means the dominance of one member of the pair across the entire biosphere. However, there is an important shortcoming in For instance in our cells, biochemical reaction networks the common discussions addressing the issue of only involve left-handed (L-chiral) amino-acids and right- homochirality namely that they only consider a small handed (D-chiral) sugars, but the reason for this absolute number of chiral− species, as in Frank's classic model [4], specificity escapes us and is one of the most fascinating or in its first experimental realization more than forty questions in the origin of life. years later by Soai et al. [16]. There is no reason to The origin of homochirality comes with two questions expect that the prebiotic world, in which homochirality and related observations: what caused the initial biais of first emerged, had such a simple and homogeneous chem- one enantiomer over the other in the presumably racemic ical composition. Instead, it is more natural to assume environment of the prebiotic world and how was this that this composition was complex, heterogeneous and bias sustained and maintained as in today's biological included a large number of chiral and achiral species. We world [1] ? It is believed that mineral surfaces on earth [2] show in this paper that generic non-equilibrium reaction or circularly polarized light in interstellar space [3] could networks possess a phase transition towards a homochi- explain the first observation, while models based on non- ral state as a consequence of the fact that the number of equilibrium reaction networks can explain the second ob- chiral species becomes large. 1 Cross-Over between chiral and achiral breaking. chemical worlds Table 1: Positions of the cross-over n1 and n2, measured With this aim, we first ask how abundant are chiral in terms of number of carbon atoms, in the study of alka- species in the chemical universe of all possible molecules? nes and monosubstituted alkanes, or in terms of number It turns out that chirality is rare among molecules with a of heavy atoms in the other studies. The estimate n1 small number of atoms, but that possible chiral stereoiso- (resp. n2) is obtained by counting once (resp. twice) the mers multiply as their number of atoms increases. Ac- pairs of enantiomers. cordingly, we should expect a cross-over between the achiral world of small molecules and the chiral world of Data n1 n2 large molecules involved in chemical reaction networks. monosubstituted alkanes stereoisomers 5.7 4.7 The cross-over should be characterized by some specific alkanes stereoisomers 9.5 8.4 number of atoms where the fractions of achiral and chi- Chemical Universe 8.5 PubChem database using raw data 9.4* − ral molecules become equal, as schematically depicted in − (Fig. 1a). Beyond the cross-over, the chiral molecules PubChem database using generated are dominant over achiral ones. The issue of this cross- enantiomers 12.7 6.7 over is important, in particular, because it associates the PubChem database using generated emergence of homochirality with some molecular size. stereoisomers 8.1 6.4 ∗ Starting with monosubstituted alkanes and alkanes for The cross-over for PubChem raw data occurs between which an exact enumeration of stereoisomers is avail- n1 and n2 because not all enantiomers of a given able [17, 18], we find that the cross-over measured in species are present in the database. number of carbon atoms in these molecules, lies between 4:7 and 5:7 for monosubstituted alkanes, and between 8:4 and 9:5 for alkanes. Spontaneous symmetry breaking into a In the chemical universe of Fink and Reymond [19], chiral state which contains all virtual molecules of a given number We now come to our central point namely, on how to of heavy atoms (i.e. atoms heavier than hydrogen) and − satisfying some basic set of rules of chemistry, we find a explain the emergence of homochirality from the mul- cross-over at 8:5 heavy atoms. Since a similar study was tiplication of chiral species in non-equilibrium reaction not available for real molecules, we turn to the chemical networks. Specifically, we consider a reaction network database PubChem [20]. From the raw data of this large involving achiral and chiral species described by the con- database, we find that a cross-over occurs for molecules centration vector c, which contains the vector cD (resp. of 9:4 heavy atoms (SI Appendix, section S1). How- cL) for the NC D-enantiomers (resp. for the NC L- ever, since many chiral molecules do not have all their enantiomers) and the vector cA for the remaining NA enantiomers or stereoisomers, we have also analyzed an achiral species. In such a system, the evolution of the expanded database, in which every chiral molecule con- concentrations is ruled by tains either all its enantiomers or all its stereoisomers. dc 1 In Fig. 1b, the fractions of chiral and achiral species are = F(c) + (c0 c) ; (1) dt τ − shown for the case of the database expanded in stereoiso- mers. Our results for the various estimates for the cross- where c0 is the concentration vector of the species sup- over are gathered in Table 1 and extracted from Fig. 1b plied from the environment at the rate 1/τ and re- and SI Appendix, Figs. S1, S2, S3 and S4. Remarkably, sponsible for driving the system out of equilibrium and irrespective of the precise procedure to generate and an- F(c) = ν w(c) are the reaction rates with specific chiral · alyze the database and regardless of the precise composi- symmetry (Eq. (14) in Materials and Methods), which tion of the molecules, the cross-over between the achiral need not obey mass-action law. In this expression, ν is and chiral worlds occurs for a number of heavy atoms the matrix of stoichiometric coefficients, w(c) the set of of the order of about 10. The main consequence of this net reaction rates. After reaction, the species in excess cross-over is that the stereoisomer distribution goes from are flowing out of the system at the same rate 1/τ as for unimodal (with a maximum for achiral molecules) to bi- the supply, so that τ represents the mean residence time modal (with maxima for opposite enantiomers) as the of the species in the system. length of molecules increases. This emerging bimodal- The stability of these equations may be characterized ity is potentially susceptible to induce a chiral symmetry by linearizing them about the racemic state, which is 2 0.5 fractions 1 L enantiomers 0 0.5 numbers of atoms achiral 0 molecules D enantiomers 0 Figure 1: Cross-over between the achiral and chiral chemical worlds. (a) A three-dimensional schematic represen- tation of the fractions of possible achiral and chiral molecules as function of their number of atoms.
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