life Review

Molecular Asymmetry in Prebiotic Chemistry: An Account from Meteorites Sandra Pizzarello School of Molecular Sciences, Arizona State University, Tempe, AZ 85287, USA; [email protected]; Tel.: +1-480-965-3370 Academic Editors: Pier Luigi Luisi and David Deamer Received: 8 February 2016; Accepted: 7 April 2016; Published: 13 April 2016

Abstract: Carbonaceous Chondrite (CC) meteorites are fragments of asteroids, solar planetesimals that never became large enough to separate matter by their density, like terrestrial planets. CC contains various amounts of organic carbon and carry a record of chemical evolution as it came to be in the Solar System, at the time the Earth was formed and before the origins of life. We review this record as it pertains to the chiral asymmetry determined for several organic compounds in CC, which reaches a broad molecular distribution and enantiomeric excesses of up to 50%–60%. Because homochirality is an indispensable attribute of extant polymers and these meteoritic enantiomeric excesses are still, to date, the only case of chiral asymmetry in organic molecules measured outside the biosphere, the possibility of an exogenous delivery of primed prebiotic compounds to early Earth from meteorites is often proposed. Whether this exogenous delivery held a chiral advantage in molecular evolution remains an open question, as many others regarding the origins of life are. Keywords: meteorites; asteroids; abiotic; prebiotic; chemical evolution; enantiomeric excess

1. Carbon-Containing Meteorites and Cosmochemical Evolution One of the paradigms of chemical evolution proposes that the abiotic formation of increasingly complex molecules throughout cosmochemical and Earthly processes could eventually lead to life’s precursor molecules. It finds its rationale in the observation of phenomena, both leading to, and proceeding from, the origin of life, such as the formation of complex organic molecules in interstellar media (e.g., [1]), and a terrestrial phylogeny that evolved from much simpler organisms (e.g., [2]). To date, such chemical evolution has found direct experimental scrutiny, solely through the analyses of Carbonaceous Chondrites (CC) meteorites, stony fragments of asteroids containing abundant organic carbon, ranging in complexity from kerogen-like macromolecular materials to simple soluble compounds, several of which are identical to terrestrial biomolecules. Because CC Asteroidal parent bodies are planetesimals found between Mars and Jupiter that never accreted large enough to undergo the extensive differentiation involved in planet formation, their meteoritic fragments uniquely offer a pristine record of abiotic organic chemistry in the early Solar System, as found in a planetary setting, at a unique juncture in the long history of the biogenic element, and at its closest to the onset of life. Their studies, therefore, have offered an understanding, not only of how compounds identical to life’s molecules were formed abiotically, but also about the organic inventory accreted by early Earth, e.g., through its heavy bombardment from comets and meteorites [3,4]. Comprehensive molecular and isotopic analyses for over forty-five years, and continuing today, have revealed that CCs may contain a complex organic suite of compounds, which are seen as the products of the synthetic capabilities of both solar and pre-solar environments [5]. Their complex range varies from polar compounds, such as amino acids, to non-polar hydrocarbons (e.g., [5–7]) and, when detected simply by their elemental compositions, may include thousands of molecular species [8]. From the perspective of a possible continuity between cosmochemical and prebiotic Life 2016, 6, 18; doi:10.3390/life6020018

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evolution, this diverse suite would not appear to indicate any selective synthetic trend and, in fact, indicate a fundamental distinction between abiotic and biological chemical processes in their gaining of molecular complexity. To say it with the words of Shakespeare, therefore, a meteoritic organic input of thousands H, C, N, O containing molecules would have offered “too much of a good thing” for an evolutionary transition towards the origins of life. Nevertheless, within this evident heterogeneity, several meteoritic compounds have been found to contain L-enantiomeric excesses (ee), i.e., to be more abundant in the L-chiral form like the amino acids of terrestrial proteins [9], offering the first unequivocal indication that a purely chemical evolutionary process, as the one believed to be responsible for the formation of meteorite organics, may also have been at work in chiral selection, a property known since the time of Pasteur to be intimately associated with life. The following review reports on ee distributions found within meteorite organics so far, the possible venues that might have lead to their formation, and the effect that the input of such selected molecules might have had in prebiotic chemistry. 2. Enantiomeric Excesses in Meteoritic Compounds The search for chiral asymmetry in meteorites was first undertaken by Engel and Nagy [10] and, although carried out carefully, was controversial [11] because of the pervasive distribution of homochirality in the biosphere and the possibility of terrestrial contamination in carbonaceous meteorites resulting from bacteria, molds, or their remnants. However, ee were ultimately detected in the Murchison meteorite for some amino acids not common in terrestrial proteins and abundant in meteorites, the 2-methyl, 2-aminoacids (2maa), and to have the same configuration (L) as protein amino acids [9]. To date, L-ee have been detected for a number of amino acids, as well as other compounds, and their inventory is summarized in Table 1 [12]. As shown, the larger number comprises the amino acids of several meteorites and involves molecular species that lack an α-H, with the exception of the diastereomers of isoleucine, as further detailed below, and the one-time finding for aspartic acid [13]. Lactic acid is the only hydroxy acid to display ee [14], while two recent communications have reported their detection in several sugar acids derivatives [15] and two amines, sec-butyl- and 1-methylbutyl amines [16]. These latter studies, appear to point at the possibility of diverse asymmetric effects in cosmochemistry. These meteoritic enantiomeric excesses are still, to date, the only case of molecular asymmetry measured outside the biosphere. The overall extent of ee in 2maa varies significantly, between 0% and 18%, and even within short distances in the same meteorite stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), the most abundant of the acids, the absence of any contribution from terrestrial contaminants within this chiral heterogeneity was validated by Murchison, using 13 C-, and D isotopic analyses [17–19], where the two enantiomers were found to have comparable enrichments. Isovaline δD values were particularly high, +3600‰ [19], and near to those measured spectroscopically for organic molecules in the interstellar medium. It should be noted that racemization, the conversion of one enantiomer into another, is possible for 2H-amino acids in water through a repeat statistical abstraction and reacquisition of the α-H and because of its vicinity to the electron-withdrawing carboxyl group. Racemization, with time and proper conditions, will lead to racemic solutions (equal amounts of the two enantiomers). The fact that all amino acids found non-racemic in meteorites have a 2-methyl in place of a 2-H and cannot racemize, easily raises the question of whether the twelve racemizable meteoritic amino acids detected having terrestrial protein counterparts might have initially carried ee but racemized during the water phases known to have affected CC parent bodies. The understanding of the processes involved in meteoritic amino acids’ syntheses and the apparently odd ee findings for diastereomer amino acids in several meteorites may be able to address the question.

compounds, and their inventory summarized in [12].same shown, theaslarger number acids [9]. date, L-ee haveis been detected forTable number ofAs amino acids, well other in meteorites, theTo 2-methyl, 2-aminoacids (2maa), and toa have the configuration (L)and asas protein withamino the exception of the diastereomers of isoleucine, as 1further detailed below, the one-time comprises the amino acids of several meteorites and involves molecular species that lack another α-H, compounds, and their inventory is summarized in Table 1 [12]. As shown, the larger number amino [9]. To date, haveacid beenisdetected a number of to amino acids,eeas wellwhile as finding foracids aspartic acid [13].L-ee Lactic the onlyforhydroxy acid display [14], two recent with the exception of reported the diastereomers of isoleucine, as further detailed below, and the comprises theand amino acids of several meteorites and involves molecular species that lackone-time an α-H, compounds, their inventory is summarized in 1 [12]. As acids shown, the larger number communications have their detection in Table several sugar derivatives [15] and two finding aspartic acid acid isofthe onlyand hydroxy acidmolecular to displayspecies ee [14],and while two with thefor exception of the[13]. diastereomers isoleucine, as further detailed below, the one-time comprises the amino acids ofLactic several meteorites involves that lack anrecent α-H, amines, sec-butyl- and 1-methylbutyl amines [16]. These latter studies, appear to point at the communications have reported their inhydroxy several sugar acids derivatives [15] and two finding aspartic acid [13]. Lactic aciddetection isofthe only acid to display ee [14],and while recent with thefor exception of the diastereomers isoleucine, as further detailed below, thetwo one-time possibility ofsec-butyldiverse asymmetric effectsamines in cosmochemistry. These meteoritic enantiomeric excesses Life 2016, 6, 18 have amines, and 1-methylbutyl [16]. These acid latter appear to[15] point the communications their inhydroxy several sugartostudies, acids derivatives andat two finding for aspartic acidreported [13]. Lactic aciddetection is the only display ee [14], while two recent are still, to date, the only case of molecular asymmetry measured outside the biosphere. possibility of diverse asymmetric effectsdetection in cosmochemistry. These meteoritic enantiomeric excesses amines, sec-butyland 1-methylbutyl amines [16]. These latter appear to [15] point at two the communications have reported their in several sugar studies, acids derivatives and are still, to date, theand only case of molecular measured outside theappear biosphere. possibility of diverse asymmetric effectsamines in asymmetry cosmochemistry. These meteoritic enantiomeric amines, sec-butyl1-methylbutyl [16]. These latter studies, to pointexcesses at the Table 1. Amines and amino-, hydroxy, and sugar-acids displaying enantiomeric in Table Amines and amino-, hydroxy, and sugar-acids displaying excesses in are still, 1. to date, the only case of molecular measured outside theenantiomeric biosphere. possibility of diverse asymmetric effects in asymmetry cosmochemistry. These meteoritic enantiomeric excessesexcesses Table 1. Amines and amino-, hydroxy,asymmetry and sugar-acids displaying enantiomeric excesses in carbonaceous chondrites. carbonaceous chondrites. are still, to date, the only case of molecular measured outside the biosphere. carbonaceous chondrites. Table 1. Amines and amino-, hydroxy, and sugar-acids displaying enantiomeric excesses in

Compound Formula carbonaceous chondrites. Table 1. Amines and amino-, Compound Formula Compound Formula carbonaceous chondrites. Compound Formula Compound Formula NH 22 NH NH2 NH2 OO

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O OH OH NH NH2O 2OH NHO O 2OH NHO2 OH OH NH O 2OH NHNH 2 O2 OH O O2 OH NH NH 2OH O OH NHNH 2 2OH NH2

O O

Compound Distribution 1 hydroxy, and sugar-acids displaying ee% enantiomeric excesses2 inDistribution 2 Compound 1 ee% 1

Compound Compound Compound Sec-butylamine Sec-butylamine Sec-butylamine

Sec-butylamine Sec-butylamine

2

ee% Distribution GRA 95229 3,* ee% 1 Distribution GRA 95229 3,* 2 GRA 95229 3, * LAP 02342LAP 02342 ee% 1 (S)(S) Distribution LAP95229 023423,* 2 GRA (S) MIL3,*07525MIL 07525 MIL95229 07525 LAP 02342 0-18GRA 0-18 (S) 0-18 PCA 91082PCA 91082 PCA 91082 MIL 07525 LAP 02342 0-18 (S) EET 92049 PCA 91082 MIL 07525 EET 92049EET 92049 0-18

EET 92049 PCA 91082

L L MN, MY *, Or 2amino2methylbutanoic a. 4 a. 4 MN, MY5 *, Or 5 2amino2methylbutanoic EET 92049 5 6,* 5 4 4 (isovaline) 2.5-19.6 LAP02342 L MN, MY *, Or 2amino2methylbutanoic a. L MN, 2amino2methylbutanoic a. 6,* MY *, Or (isovaline) 2.5-19.6 LAP02342 6,

(isovaline) (isovaline) 2amino2methylbutanoic a. 4 2amino2methylpentanoic (isovaline) 2amino2methylpentanoic (2methylnorvaline) 2amino2methylpentanoic (2methylnorvaline) (2methylnorvaline) 2amino2methylpentanoic 2amino2methylpentanoic 2amino2methylhexanoic (2methylnorvaline) (2methylnorvaline) 2amino2methylhexanoic (2methylnorleucine) 2amino2methylhexanoic (2methylnorleucine) 2amino2methylhexanoic (2methylnorleucine) (2methylnorleucine) 2amino2methylhexanoic (2methylnorleucine)

6,* 5 LAP02342 * 2.5-19.6 LAP02342 L 2.5-19.6 MN, MY *, Or L 6,* 2.5-19.6 LAP02342 MN, MY L 1.4-2.8 L MN, MY MN, MY 1.4-2.8 L 1.4-2.8 L MN, MY L 1.4-2.8 MN, MY 1.4-2.8 MN, MY 1.8 L L MN, MY MN, MY 1.8 L 1.8 MN, MY 1.8 L 3 of 9 MN, MY 3 of 9 1.8

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2amino2methylheptanoic L MN 3 of 9 OH 2amino2methylheptanoic L MN O OH NH 2 Life 2016, 6, 18 3 of 9 MN 2amino2methylheptanoic L NH 2amino2methylheptanoic L MN O O 2OH MN, MY Life 2016, 6, 18 3 of 9 O MN, MY 2amino3methylpentanoic L NH 2 O 2amino2methylheptanoic MN OHOH 2amino3methylpentanoic L Life 2016, 6, 18 3 of 9 GRA 95229 OH MN, MY GRA 95229 (isoleucine) 4-50 MN, MY NH2ONH O 2OH 2amino2methylheptanoic L MN Life 2016, 6, 18 3 of 9 2amino3methylpentanoic L LAP (isoleucine) 4-50 02342 2amino3methylpentanoic L NH2 GRA 95229 LAP 02342 OH ONH 95229 O 2OH 2amino2methylheptanoic L MN O MN, MY (isoleucine) 4-50 GRA MN, MY Life 2016, 6, 18 3 LAP of 9 02342 (isoleucine) 4-50 O 2amino3methylpentanoic L NH2O MN, MY 2amino3methylpentanoic D NH O LAP 02342 MN, MY 2amino2methylheptanoic L MN OH GRA 95229 OH2OH 2amino3methylpentanoic D GRA 95229 2amino3methylpentanoic L (isoleucine) 4-50 OH2 NH2ONH GRA 95229 (alloisoleucine) 2-60 2amino2methylheptanoic L MN OH MN, MY GRA 95229 H2N O OH LAP 02342 (alloisoleucine) 2-60 LAP 02342 2amino3methylpentanoic L D H2N (isoleucine) 4-50 NH2O NH LAP 02342 MN, MY MN, MY GRA 95229 LAP 02342 MN, MY OO OH2OH 2amino2methylheptanoic L MN 2amino3methylpentanoic D 2amino3methylpentanoic L (isoleucine) 4-50 (alloisoleucine) 2-60 O OH 2amino3methylpentanoic D NHO H2N 2amino2,3methylbutanoic L 2O MN,02342 MY GRA 95229 GRA 95229 NH LAP OH MN, MY 2 GRA 95229 2amino2,3methylbutanoic L OH (alloisoleucine) 2-60 MN, MY 2amino3methylpentanoic L (isoleucine) 4-50 2amino3methylpentanoic D (alloisoleucine) 2-60 (2methylvaline) 1.0 2 OOH OH LAP 02342 O N NH H2NH GRA 95229 LAP GRA 95229 MN,02342 MY 2 OH LAP 02342 (2methylvaline) 1.0 2amino2,3methylbutanoic L (isoleucine) 4-50 NH D NH 2amino3methylpentanoic L (alloisoleucine) 2-60 2O H2N O LAP 02342 MN, MY O2OH OH GRA 95229 LAP 02342 (2methylvaline) 1.0 O 2amino3methylpentanoic D 2amino2,3methylbutanoic L (alloisoleucine) 2-60 (isoleucine) 4-50 O N NH H2NH O MN,02342 MY 2 2 OH L 2amino2,3methylpentanoic GRA 95229 LAP OH OH 2amino3methylpentanoic D 2amino2,3methylpentanoic MN, MY 2amino2,3methylbutanoic L 1.4-5.2 (alloisoleucine) 2-60 (2methylvaline) 1.0 2amino2,3methylbutanoic L GRA O OH OH H2N NH NH O O2OH 95229 2 1.4-5.2 MN, MY LAP 02342 MN, MY L MY NH2 2amino2,3methylbutanoic L (alloisoleucine) 2-60 (2methylvaline) 1.0 (2methylvaline) 1.0 MN, 2amino2,3methylpentanoic MN,02342 MY 2amino3methylpentanoic D H2N NH OH OO2OH MN, MY LAP OH 1.4-5.2 GRA 95229 O allo L 2amino2,3methylbutanoic (2methylvaline) 1.0 NH2 (alloisoleucine) 2-60 allo L OO2OH 2amino2,3methylpentanoic H2N NH MN, MY OH LAP L MN,02342 MY 2amino2,3methylpentanoic 2.2-10.4 1.4-5.2 2amino2,3methylbutanoic O OH (2methylvaline) 1.0 O NH NH 2amino2,3methylpentanoic MN, MY 2.2-10.4 2OH 2OH allo L O NH2 L 1.4-5.2 L (2methylvaline) 1.0 MN, MY MY O 2amino2,3methylbutanoic L NH OH O2 2O NH 2amino2,3methylpentanoic MN, 2amino2,3methylpentanoic MN, MY OH 2amino2,3methylpentanoic 2.2-10.4 O O MY L 1.4-5.2 MN, allo 1.4-5.2 NH 2 OOH NH L (2methylvaline) 1.0 2methylglutamic MN 2amino2,3methylpentanoic MN, MY 2 HO OH OH NH2 allo L 2methylglutamic MN 3-2 2amino2,3methylpentanoic 2.2-10.4 O OH 1.4-5.2 HO O ONH NH MN, MY 2 3-2 2amino2,3methylpentanoic 2OH L ONH allo L 2 2amino2,3methylpentanoic 2.2-10.4 1.4-5.2 2methylglutamic MN 7,*, L HO O ONH OH O 2O MN MN, MY OH 3-2 O NH 7,*, 2amino2,3methylpentanoic OH allo L MN MY 2amino2,3methylpentanoic 2.2-10.4 allo L MN, 2 O O 1.4-5.2 O NH 2methylglutamic MN MN, MY 2 L GRA95229 * Lactic OH MN, MY HO OH NH 2OH L 2.2-10.4 allo 3-2 O OH 2amino2,3methylpentanoic 2.2-10.4 7,*, * 2amino2,3methylpentanoic GRA95229 Lactic 3.0-12-3 MN NH 2methylglutamic MN MN, MY 2O 2OH HO O OH NH 3.0-12-3 LAP 02342 * L OH O OH 3-2 2amino2,3methylpentanoic 2.2-10.4 LAP 02342 allo L 7,*, * GRA95229 * Lactic OH O 2OH 2methylglutamic MN MN 2 ONH HO O OHONH MN, MY 3.0-12-3 OH L 3-2 OH OHO ONH 7, 2amino2,3methylpentanoic 2.2-10.4 O O LAP 02342 MN 2methylglutamic MN 8*, ** 2OH GRA95229 Lactic OH HO Threonic D MN NH 2OH HO 8 L 3-2 L 3.0-12-3 Threonic D MN O 7,*, OH O OH NH OH 2methylglutamic HO MN 2methylglutamic MN GRA95229 * Lactic HO O LAPMN 02342 OHOHO 2OH 3-2 L 3-2 3.0-12-3 OH L 8 7,*, OHO Threonic MN 2 1 Values HO 2 Meteorites where ee D MN OH GRA95229 * are Lactic ONH OH OH LAP 02342 from [12] unless otherwise indicated; of the given compounds 2methylglutamic MN HO OH 1 Values from [12] unless otherwise indicated; 2 Meteorites where3.0-12-3 Lof the given compounds ee3-2 O 7,8*, OH OH MN OH ONH GRA95229 * are Lactic OH LAP 02342 D MN found. MN, Murchison; MY, Murray; Threonic Or, Orgueil; * isotopic data acquired for individual 2 OH HO Murchison; L acquired 3.0-12-3 found. MY, Murray; Or, Orgueil; * isotopic data for individual 1 ValuesMN, 2 OH from [12] unless Meteorites where ee D of the given compounds are OH MN 7, *, O OH GRA95229 Lactic 3O 4 acid; 5otherwise 7 [14]; 8 [15], 7,8*, *sugar OH Threonic MN LAP 02342 OH [18]; 6 [39];indicated; this last study detected other ee-containing enantiomers; MN HO 3 [16]; L ee-containing 4 acid; 5 [18]; 6 [39]; 7 [14]; 8 [15], this last study detected 3.0-12-3 [16]; other sugar enantiomers; L OH 8 MY, Murray; Or, Orgueil; * isotopic acquired for individual 1found. 2 Meteorites Lactic OHMurchison; O OH LAP 02342 OH Threonic D MN ValuesMN, from [12] unless otherwise indicated; where eedata of the given compounds acids. GRA95229 ** are GRA95229 * Lactic OH HO 3.0-12-3 3 [16]; 4 acid; 5 [18]; 6 [39]; 7 [14]; 8 [15], 3.0-12-3 8 1acids. 2 Meteorites OH this last study detected other ee-containing enantiomers; O OH OH Threonic D MN ValuesMN, from [12] unless otherwise indicated; where ee of the given compounds are LAP 02342 * OH found. Murchison; MY, Murray; Or, Orgueil; * isotopic data acquired for individual LAP 02342 *sugar HO 8 1 2 acids. 3 4 5 6 7 8 Threonic D MN OH Values from [12] unless Meteorites where ee of the given compounds are found. MN, Murchison; MY, Murray; Or,significantly, Orgueil; * study isotopic data acquired for individual [16]; acid; [18]; [39];indicated; [14]; [15], this last detected other ee-containing sugar enantiomers; The overall of ee otherwise in 2maa varies between 0% and 18%, and even within OHextent O OH HO The overall extent of ee in 2maa varies significantly, between 0% and 18%, and even within 2 Meteorites 3 Murchison; 4 acid; 5otherwise 7 [14]; 8 [15], OH ValuesMN, from [12] unless indicated; where eedata of the given compounds areacid), found. MY, Or, Orgueil; * study isotopic acquired for individual 8 [16]; [18]; 6Murray; [39];stone this last detected other ee-containing sugar acids. short1enantiomers; distances in the same meteorite [17,18]. For Isovaline (2-amino, 2-methylbutanoic Threonic D MN OH HO inextent shortfound. distances the same stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), 1The 2 overall of eemeteorite in 2maa varies between 0% and 18%, and even within 4 acid; 5otherwise 6Murray; 7 [14]; 8significantly, Values from3Murchison; [12] where ee of the given compounds are MN, MY, Or, Orgueil; * isotopic data acquired for individual [16]; [18]; [39];indicated; [15], this study detected other ee-containing sugar enantiomers; acids. the most abundant ofunless the acids, the absence ofMeteorites anylast contribution from terrestrial contaminants OH Threonic D MN 8 the most abundant of the acids, the absence of any contribution from terrestrial contaminants 3extent 4 acid; 5 MY, 6Murray; 7 [14]; 8significantly, short distances in the same meteorite stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), found. MN, Murchison; Or, Orgueil; * isotopic data acquired for individual 13 The overall of ee in 2maa varies between 0% and 18%, and even within acids. [16]; [18]; [39]; [15], this last study detected other ee-containing sugar enantiomers; 1 2 withinValues this1 chiral heterogeneity was validated byMeteorites Murchison, using C-, and Dcompounds isotopic analyses from [12] unless otherwise indicated; where ee of13ee the are are found. MN, 2 Meteorites Values from [12] unless otherwise indicated; where ofgiven the given compounds within this chiral heterogeneity was validated by Murchison, using C-, D isotopic analyses 4 acid; 5 in 6 the 7 [14]; 8significantly, the most abundant ofsame the acids, absence of any contribution from terrestrial contaminants The overall of eemeteorite 2maa varies between 0% andand 18%, and even [16]; [18]; [39]; [15], this last detected other ee-containing sugar enantiomers; acids. short distances in3extent the stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), 3within 4 5 found. MN,the Murchison; MY, Murray; Or, Orgueil; * study isotopic data acquired for individual [17–19], where two enantiomers were found have comparable enrichments. Isovaline δD values were Murchison; MY, Murray; Or, Orgueil; * to isotopic data acquired for individual enantiomers; [16]; 13C-, [17–19], where the two enantiomers were found to by have comparable enrichments. Isovaline δD values were acid; [18]; within this heterogeneity was validated Murchison, using and D isotopic analyses 6 chiral 7 8 The overall extent of ee in 2maa varies significantly, between 0% and 18%, and even within acids. short distances in the same meteorite stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), 3 4 5 6 7 8 the most abundant of the acids, the absence of any contribution from terrestrial contaminants [39];+3600‰ [14]; acid; [15], last study detected other ee-containing sugarother acids. [16]; [18]; [39]; this last study detected sugar in enantiomers; particularly high, [19],this and near to[14]; those[15], measured spectroscopically foree-containing organic molecules particularly high, +3600‰ [19], and2maa near to those spectroscopically for organic molecules in 13C-, The overall extent of eemeteorite in varies significantly, between 0% andand 18%, andδD even within [17–19], where the two enantiomers were found tomeasured have comparable enrichments. Isovaline values were short distances in the stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), the most abundant ofsame the acids, the absence of any contribution from terrestrial contaminants within this chiral heterogeneity was validated by Murchison, using D isotopic analyses acids. the interstellar medium. the interstellar medium. 13 The overall extent of ee in 2maa varies significantly, between 0% and 18%, and even within short in the meteorite stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), particularly high, +3600‰ [19], andwas near to those spectroscopically for organic molecules in the most abundant ofsame the acids, the absence of any contribution from terrestrial contaminants within this chiral heterogeneity validated by Murchison, C-, and Danother, isotopic [17–19], where the two enantiomers were found tomeasured have comparable enrichments. Isovaline δD values were Itdistances should be noted that racemization, the conversion of one using enantiomer into is analyses possible Itdistances should be noted that racemization, the[17,18]. conversion of one using enantiomer into another, is analyses possible 13C-, and short in the same meteorite stone For Isovaline (2-amino, 2-methylbutanoic acid), the most abundant of the acids, the absence of any contribution from terrestrial contaminants interstellar medium. within this chiral heterogeneity was validated by Murchison, D isotopic [17–19], where the two enantiomers were found to have comparable enrichments. Isovaline δD values were The overall extent of ee in 2maa varies significantly, between 0% and 18%, and even within particularly high, +3600‰ [19], and near to those measured spectroscopically for organic molecules in for 2H-amino acids in water through a repeat statistical abstraction and reacquisition of the α-H and 13C-, for 2H-amino acids inofsame water through avalidated repeat statistical abstraction and reacquisition of the α-H and the most abundant the acids, the absence of any contribution from terrestrial contaminants within this chiral heterogeneity was by Murchison, using and Danother, isotopic analyses Itdistances should be noted that racemization, the conversion of onegroup. enantiomer into istime possible [17–19], where the two enantiomers were found tomeasured have comparable enrichments. Isovaline δD values were particularly +3600‰ [19], and near to those spectroscopically for organic molecules in short in the meteorite stone [17,18]. For Isovaline (2-amino, 2-methylbutanoic acid), the interstellar medium. because of high, its vicinity to the electron-withdrawing carboxyl Racemization, with and 13C-, and D isotopic because of its vicinity to the electron-withdrawing carboxyl group. Racemization, with time and within this chiral heterogeneity was validated by Murchison, using analyses [17–19], where the two enantiomers were found to have comparable enrichments. Isovaline δD values were for 2H-amino acids in water through a repeat statistical abstraction and reacquisition of the α-H and particularly high, +3600‰ [19], and near to those measured spectroscopically for organic molecules in interstellar medium. the most abundant of the acids, the absence of any contribution from terrestrial contaminants It should be noted that racemization, the conversion of one enantiomer into another, is possible proper conditions, will lead to racemic solutions (equal amounts of the two enantiomers). The fact proper conditions, will lead to racemic solutions (equal amounts ofand the two enantiomers). Thewere fact [17–19], where the two enantiomers were found tomeasured have comparable enrichments. Isovaline δD values 13C-, particularly high, +3600‰ [19], and near to those spectroscopically for organic molecules in because of its vicinity to the electron-withdrawing carboxyl group. Racemization, with time and the interstellar medium. It should be noted that racemization, the conversion of one enantiomer into another, is possible within this chiral heterogeneity was validated by Murchison, using and D isotopic analyses for 2H-amino acids in water through a repeat statistical abstraction reacquisition of the α-H and that all amino acids found non-racemic in meteorites have a 2-methyl in place of a 2-H and cannot Life 2016, 6, 18

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A possible pathway proposed for the formation of 2-amino-, and 2-hydroxy acids in meteorites is the addition of ammonia and HCN to ketones and aldehydes in the presence of water (Figure 1a, Reference [12] and the references therein). This is a reasonable hypothesis, for at least some of the amino acids because all the needed reagents are abundant components of interstellar ices and likely Life 2016, 6, 18 4 of 9 constituents of primitive asteroids [20,21]. Although producing an asymmetric carbon and, therefore, a chiral molecule in most cases, this type of synthesis is non-stereospecific because the HCN addition therefore, a chiral molecule in most cases, this type of synthesis is non-stereospecific because the would be random give amounts D-, amounts and L-enantiomers. HCN addition and would be equal random and giveof equal of D-, and L-enantiomers.

Figure 1. (a) The Strecker synthesis for the possible formation of amino acids in meteorites ([12] and

Figure 1. (a) The Strecker synthesis for the possible formation of amino acids in meteorites ([12] references therein); (b) Structural relation of the alloisoleucine and isoleucine diastereomers; (c) and references therein); (b) Structural relation of the alloisoleucine and isoleucine diastereomers; Enantiomeric excesses detected for the isoleucine diastereomers in the GRA 95229 meteorites using (c) Enantiomeric excesses detected for the isoleucine in the GRA 95229 meteorites using Gas Chromatography-Mass Spectrometry, single iondiastereomers traces [22]. Gas Chromatography-Mass Spectrometry, single ion traces [22]. However, reaction products become more complex for longer aldehydes that already contain an asymmetric carbon, such as in the synthesis of the 6-C isoleucine (ile) and alloisolucine (allo) diastereomers (Figure 1b) from DL 2-methylbutanal [12]. In this case, were an ee already present in

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However, reaction products become more complex for longer aldehydes that already contain theasymmetric precursor aldehyde, e.g., of those product amino acids(allo) that an carbon, such asthe in (S) theconfiguration, synthesis of the 6-Cdiastereomeric isoleucine (ile) and alloisolucine carried the (S) portion of the precursor through their synthesis will be more abundant than their diastereomers (Figure 1b) from DL 2-methylbutanal [12]. In this case, were an ee already present in the respectivealdehyde, enantiomers any ee would be revealed in different compounds. precursor e.g., and of the (S)original configuration, those diastereomeric product amino acids that carried Inportion the above example, thisthrough would be thesynthesis (RS) allo and ile compounds or, intheir the respective formalism the (S) of the precursor their will (SS) be more abundant than used for amino acids, D -allo and L -ile. As can be seen, these two sets of diastereomers are also each enantiomers and any original ee would be revealed in different compounds. other’s racemization product (calledbeepimerization in (SS) this ile case,) and, because theformalism 3C is too far In the above example, this would the (RS) allo and compounds or, in the used removed from the carboxyl and will racemize much more slowly, if at all, original ee may be for amino acids, D-allo and L-ile. As can be seen, these two sets of diastereomers are also each other’s preserved much longer. racemization product (called epimerization in this case,) and, because the 3C is too far removed from Such was distribution foundmore in the extracts group of meteoritesmuch collected in the carboxyl andthe will racemize much slowly, if at of all,a original ee pristine may be preserved longer. Antarctica (Renazzo-type or CR) (Figure 1c, [22,23]) and, based on the above formative premise, as Such was the distribution found in the extracts of a group of pristine meteorites collected in well as upon confirmingor the indigeneity all four individual by 13C isotopic Antarctica (Renazzo-type CR) (Figure 1c,of[22,23]) and, based onenantiomers the above formative premise,analyses as well [22], theconfirming findings were interpretedoftoallsignify that theirenantiomers precursor aldehyde carriedanalyses an original as upon the indigeneity four individual by 13 C isotopic [22], S-asymmetry to the meteorite’s parent body. CR meteorites’ organic composition, therefore, offers the findings were interpreted to signify that their precursor aldehyde carried an original S-asymmetrya new account of body. cosmochemical evolution’s capabilities toward the selective of to theexciting meteorite’s parent CR meteorites’ organic composition, therefore, offers aproduction new exciting very large abiotic ee, of up to 60% in the case of the isoleucine diastereomers, in some meteorites account of cosmochemical evolution’s capabilities toward the selective production of very large abiotic (Table ee, of up1).to 60% in the case of the isoleucine diastereomers, in some meteorites (Table 1). 3. The Likely Likely Locals Locals for for Asymmetric Asymmetric Syntheses Syntheses 3. The The in the amino acidsacids of meteorites has been debated since their initial detection, The origin originofofee ee in the amino of meteorites haslong been long debated since their initial and is still and not is known (e.g., [24]).(e.g., The [24]). first hypotheses to be put to forward their possible detection, still not known The first hypotheses be put proposed forward proposed their asymmetric decomposition upon UV upon photolysis [25] and, following hint of the amino high possible asymmetric decomposition UV photolysis [25] and, the following hintacids’ of amino isotopic enrichments deuterium, the theirlikelihood syntheses in acids’ high isotopic inenrichments in likelihood deuterium,of the of cold, theirdeuterium-enriching syntheses in cold, cosmic environments [7]. The two enantiomers[7]. of aThe chiral molecule have identical chemical properties, deuterium-enriching cosmic environments two enantiomers of a chiral molecule have but differ in some physico-chemical features, [26], and, as a result, react/interact identical chemical properties, but differ in e.g., somepolarizability physico-chemical features, e.g., may polarizability [26], differently with other molecules or entitieswith (a common illustration couldorbeentities that of (a thecommon distinct and, as a result, maychiral react/interact differently other chiral molecules illustration couldcan be that the distinct waysaims). two people can join hands for different aims). ways two people join of hands for different The effects effects of of UV UV circularly circularly polarized polarized light light (CPL) (CPL) irradiation, irradiation, which which can can have have right-handed right-handed or or The left-handed helical helicalpaths pathsofofpropagation propagation(Figure (Figure2),2), were discussed and studied in detail left-handed were discussed and studied in detail [27][27] andand for for amino in particular. experiments showirradiation UVCPL generating irradiation adsorption generating amino acids acids in particular. Several Several experiments did showdid UVCPL adsorption bands by the compounds with the sign as the irradiating CPL [28], andover evenaover bands by the compounds with the same signsame as the irradiating CPL [28], and even largea large wavelength [29], however, the maximum ee achieved found to at be,most, at most, (at wavelength range range [29], however, the maximum ee achieved werewere found to be, 9% 9% (at an an unlikely 1 [30]), far lower found in meteorites. unlikely pH pH 1 [30]), i.e., i.e., far lower thanthan found in meteorites.

Figure 2. 2. Graphic Graphic representation representation of of Left Left and and Right Right Circularly Circularly Polarized Polarized Light. Light. Figure

These experimental data leave open the possibility that ee were first formed in precursor molecules, such as the aldehydes mentioned above, which would also justify the findings for ile and allo. Aldehydes have not been studied in this regard, e.g., their circular dichroism is not known,

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These experimental data leave open the possibility that ee were first formed in precursor molecules, such as the aldehydes mentioned above, which would also justify the findings for ile and allo. Aldehydes have not been studied in this regard, e.g., their circular dichroism is not known, nor is their behavior upon CPL irradiation, and the field is, in fact, yet open to inquiry. However, the proposal of their participation as precursors to the syntheses of amino acids in meteorites would draw the important inference that, because chiral aldehydes racemize quickly in water, in fact, much more rapidly than amino acids, the synthetic window for amino acids in meteorites from non-racemic aldehydes during the asteroidal water processes should have been short and icy [22]. Early parent body aggregates or protoplanetary disc environments would fit the scenario, with ammonia abundance possibly providing a lower freezing point of water. Although the scenario also implies that meteoritic ee would be rare and could be detected for 2-amino acids only in the special cases, such as for the diastereomer compounds described above, the hypothesis does not explain the ee for 2maa, of which precursors would be ketones that cannot racemize. Additionally, the large heterogeneity of ee values demonstrated throughout these studies of meteoritic chiral compounds is very puzzling and has brought other proposals that the formation of ee could be related to asteroidal parent body effects during aqueous stages [12,31] and, in particular, catalysis from their mineral phases. This was first addressed to justify the large variability of isovaline ee between contiguous fragments of the Murchison meteorite and, by their X-ray diffraction analyses, showed a possible correlation between isovaline ee and hydrous silicates abundances [16]. In the case of CR meteorites mentioned above, that their aqueous processes are found to be variable within the meteorite matrix [31] would also satisfy the observation of varying ee detected between meteorites’ samples. The recent findings of two non-racemic amines in several CR2 meteorites with ee as high as 60% [15] were able to further this discussion. Because, as for amino acids, amines’ circular dichroism [15] and anisotropy spectra [32] do not encourage suggestions of possible asymmetric effects by UV CPL, it has been proposed that the ketones precursor to these amines, while not chiral, could have benefited by adsorption upon mineral phases possessing asymmetry. Such minerals, e.g., magnetite seen to have in meteorites helical structures [33], could then provide chiral induction during syntheses. For 2-methylamines, it could have been a reductive amination process made possible by the large abundance of ammonia known to be present in this type of meteorites, e.g., [34]. If further confirmed experimentally, processes like these would point to possible important roles for Asteroidal bodies, their aqueous history and the minerals ensuing from warm hydrous stages in the development of chiral asymmetry in prebiotic molecules. 4. Prebiotic Chiral Asymmetry and the Origins of Life The origins of life are utterly unknown, have been debated for close to a century, and the only achieved consensus is one of life likely emerging from inanimate molecules, about 3.5 billion years ago and by diverse possible scenarios, such as syntheses in the early atmosphere, the deep Earth or by input of organics materials from comets and meteorites (e.g., [5,35,36]). As mentioned already, and as Cronin and Chang [37] remarked pointedly, the known meteoritic inventory discussed above “ . . . is clearly not the recipe for constructing the progenote . . . and a basic challenge resides in finding . . . where diversity that characterizes chemical evolution . . . gives way to the selectivity of life”. The question therefore is: Has the molecular asymmetry of meteoritic compounds changed the odds of an exobiology? One distinguishing characteristic of Earth life is that the structure and functions of biopolymers rely on the exclusive one-handedness of their monomeric components, i.e., most protein amino acids have an L-configuration while sugars in RNA and DNA have a D-configuration and substitutions along the polymers with enantiomers of opposite handedness usually result in loss of function. That the trait of molecular asymmetry could be, or become by evolution, so pervasive as to define life

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processes and that several meteoritic compounds may have ee of the same L-configuration as terrestrial proteins do seem to provide a new dimension to this debate. However, the overall data also pose a caveat. As we have seen, the asteroidal aqueous environments, as recorded in the mineralogy of all meteorites containing organic compounds of prebiotic interest, tend to racemize either the α-H amino acids or their aldehyde precursors, making ee for these amino acids scarce in the mature parent bodies. The α-substituted species that do not racemize would be more abundant but possibly less reactive. On the other hand, their ketone precursors do not racemize at all and could, in fact, have been very desirable prebiotic reactants. Moreover, some of the CC meteorites, such as the Renazzo-type, contain, not only abundant amino acids, but also large abundance of ammonia [38–40], an indispensable reactant for their syntheses. The combination of mineral catalysts with exogenously delivered key ingredients and chiral compounds, therefore, may still represent a very good evolutionary chance in prebiotic chemistry. Acknowledgments: The author is grateful for the near forty years of funding from the NASA Exobiology and Astrobiology Division and the current support from the National Aeronautics and Space Administration under Agreement No. NNX15AD94G for the program “Earths in Other Solar Systems”. Conflicts of Interest: The authors declare no conflict of interest.

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