Enceladus: First Observed Primordial Soup Could Arbitrate Origin-of-Life Debate

Abstract

A recent breakthrough publication has reported complex organic molecules in the plumes emanating from the subglacial water ocean of Saturn's moon Enceladus (Postberg et al., 2018, Nature 558:564-568). Based on detailed chemical scrutiny, the authors invoke primordial or endogenously synthesized carbon-rich monomers (<200 u) and polymers (up to 8000 u). This appears to represent the first reported extraterrestrial organics-rich water body, a conceivable milieu for early steps in life's origin ("prebiotic soup"). One may ask which origin-of-life scenario appears more consistent with the reported molecular configurations on Enceladus. The observed monomeric organics are carbon-rich unsaturated molecules, vastly different from present-day metabolites, amino acids, and nucleotide bases, but quite chemically akin to simple lipids. The organic polymers are proposed to resemble terrestrial insoluble kerogens and humic substances, as well as refractory organic macromolecules found in carbonaceous chondritic meteorites. The authors posit that such polymers, upon long-term hydrous interactions, might break down to micelle-forming amphiphiles. In support of this, published detailed analyses of the Murchison chondrite are dominated by an immense diversity of likely amphiphilic monomers. Our specific quantitative model for compositionally reproducing lipid micelles is amphiphile-based and benefits from a pronounced organic diversity. It thus contrasts with other origin models, which require the presence of very specific building blocks and are expected to be hindered by excess of irrelevant compounds. Thus, the Enceladus finds support the possibility of a pre-RNA Lipid World scenario for life's origin.

Keywords: Carbonaceous chondrite; Enceladus; Lipid First model; Mutual catalysis; Origin of life; Prebiotic chemistry.

FIG. 1.

Conceptual macromolecular structures of insoluble organic matter (IOM). (A) Humic acid (∼3000 u) inferred on the basis of analytical degradation (Schulten and Schnitzer, 1993). Humic acid is a carbon- and oxygen-rich, largely unsaturated polymer, with an example empirical formula of C₁₀₀H₉₁O₄₇N₂S₁P_0.05 (Chiou et al., 1987), formed upon anoxic modification of biomatter (Quentel and Filella, 2008). In some respects, it is similar to IOM in carbonaceous meteorites (Derenne and Robert, 2010) (B), which is less reduced (C₁₀₀H₇₀O₁₂N₃S₂) (Postberg et al., 2018). This model was built from measured elemental composition and ratios of different chemical groupings. R stands for an organic moiety. Another term used for such insoluble structures is “refractory organic material” (ROM, meaning difficult to dissolve and analyze) (Quentel and Filella, 2008). Such substances are also similar to tholins, organic heteropolymeric tarry solids (Waite et al., 2007) detected, for example, in Titan's aerosols, and asphaltite-like substances observed on the asteroid Ceres (De Sanctis et al., 2017). Further, similar to humic acid, the term kerogen is frequently used for analogous insoluble organic macromolecular materials abundant in terrestrial sedimentary rocks (Vandenbroucke and Largeau, 2007), termed also sedimentary organic matter (Leif and Simoneit, 1995). Also, the term “insoluble macromolecular organic matter” (IMOM) has been used for the product of diagenetic sequestration of microbial mat lipid biomarkers through covalent binding (Lee et al 2019). Finally, comparable refractory substances are generated profusely in synthetic reactions such as the Miller-Urey electrical discharge synthetic reactions (Cleaves et al., 2014).

FIG. 2.

Organic molecules reported by astrochemical investigations. A collection of 53 neutral organic compounds that were detected in the interstellar medium or circumstellar shells (Klemperer, 2011) (Table 1). Topping the list are 35 compounds with 8 or more atoms (C, H, N, O, S). While some of these molecules are present in living cells, the overall picture is that of a random assortment of molecular structures, mostly with up to 7 carbon atoms. A complementary view is obtained from a recent direct analysis of comet 67P (Goesmann et al., 2015), showing 12 organic compounds with up to 10 atoms (C, H, N, O), seven of which overlap with the interstellar list. Monomeric organic molecules have been detected on other planetary bodies, for example, at Gale Crater on Mars, where short aliphatic compounds up to C₅ and sulfur-containing thiophenes have been recently reported (Eigenbrode et al., 2018).

FIG. 3.

Prebiotic soup in the context of possible routes to life's origin. A prebiotic soup is by definition a water body that carries dissolved or stably dispersed organic molecules, the latter being in the form of micelles, vesicles, or emulsions. The three major sources for soup compounds are infalling water-dispersible organics, infalling water-nondispersible organics that become solubilized by abiotic differentiation, and very simple compounds that undergo abiotic synthesis to both dispersible and nondispersible compounds. The RNA World scenario calls for yet another abiotic synthesis—the generation of replicating biopolymers from specific monomers in the soup, so as to jump-start an evolutionary process (Cafferty and Hud, 2014) (blue). In contrast, the Lipid World scenario posits that replication, selection, and evolution can transpire at the level of monomers, by compositional inheritance mediated by a mutually catalytic network (Lancet et al., 2018) (green). The term heterotrophy indicates that the evolving entity depends, at least partially and temporarily, on feeding on compounds from the soup. Prebiotic autotrophy (purple) is an extreme case in which the only external compounds for jump-starting life are simple molecules such as CO₂ and water, leading to adsorbed protometabolism energized by photons, temperature or ion gradients, or mineral components (Maden, 1995). In some respects, this constitutes a flat version of a prebiotic soup (von Kiedrowski, 1996). In answer to how flat metabolism would become more life-like, the answer given is mutually catalytic evolution (Huber et al., 2012), similar to what is invoked for the Lipid World.

FIG. 4.

Mass spectrum from the Cassini Cosmic Dust Analyzer (CDA), adapted from extended data Fig. 5A in Postberg et al. (2018). More details are in the text.

FIG. 5.

(A) Distribution of mass spectrometry peaks in extracts of a Murchison meteorite sample. Shown here are the molecular series of compounds containing only carbon, hydrogen, and oxygen showing the number of oxygen atoms (vertical axis) versus carbon atoms (horizontal axis). Circle areas are related to mass peak intensities; here, singular large peaks likely denote terrestrial contamination. The bulk of the compounds are C₁₂–C₃₀ with the main intensities in the O₂ row, consistent with amphiphilic character. Adapted from Fig. S8A in Schmitt-Kopplin et al. (2010). (B) Carbon atom enrichment distribution of non-sulfuric compounds extracted by methanol from a Murchison meteorite sample. Molecules labeled in green are graph positions consistent with fatty acid lipids: CA, capric acid (C₁₀); LA, lauric acid (C₁₂); PA, palmitic acid (C₁₆); SA, stearic acid (C₁₈); AA, arachidic acid (C₂₀). The double arrow indicates the approximate molecular mass range of the heavy species seen in the high-resolution part of Fig. 4. Thus, the entire range of this monomeric collection spans up to ∼700 u. (C) Intensity distribution of the Murchison compounds shown in (B). It is apparent that in the main the compounds span 1.5 orders of magnitude of concentrations.

FIG. 6.

Enceladus cross section, showing the different potential components of the soup and the plumes. IOM stands for insoluble organic matter, which is taken to be synonymous with nondispersible organic matter in Fig. 3. Such polymeric compounds can still be carried in the plume as small particles detached from insoluble organic layers at the top of the water layer. Lipid in water alludes to monomers and aggregates such as micelles and vesicles. Organic in water is dispersed, for example as microemulsion. Inspired by the data in Postberg et al. (2018).

FIG. 7.

From soup to protocells, delineating the underpinnings of two different models, RNA First (RF, top) and Lipid First (LF, bottom). In RF, specific monomers are singled out from a heterogeneous chemical mixture and undergo polymerization, culminating in the emergence of a self-replicating polymer. This is then enclosed in a lipid bilayer, leading to protocells capable of selection and evolution. In LF, a large variety of amphiphiles spontaneously generates a plethora of assemblies, for example micelles. The GARD model then predicts that very specific micellar compositions establish a mutually catalytic network, which may exhibit homeostatic growth. This, when followed by fission events, constitutes a reproduction system, capable of selection and evolution (see “How do lipids reproduce?” Section 8.4 and Lancet et al. [2018]). Subsequent prolonged evolution may lead to the emergence of RNA, proteins, and metabolism (See Section 8.5, “How would lipids beget full-fledged protocells” and Lancet et al. [2018] Section 11.1). The pros and cons of the two models are summarized herein:

1. (i)

   Compatibility with the chemical diversity: RF depends on selection or synthesis of a very specific subset of monomeric compounds, such as four nucleotide bases and the sugar ribose. Chemical diversity is an impediment, leading to side reactions and making the spontaneous emergence of nucleotides and their linear polymer less likely (Shapiro, 2000). LF is promiscuous, with amphiphile assemblies readily emerging out of a very complex monomer mixture.

2. (ii) 

   Facility of chemical reactions: RF requires covalent polymerization, necessitating activated monomers as a free energy source. LF stays away from equilibrium by spontaneous “noncovalent polymerization” toward micelle formation, an energetic downhill reaction driven by hydrophobic interactions, and via physical disruption that leads to fission.

3. (iii) 

   Need for a concentration mechanism: In RF, for a biopolymer to form, a monomer concentration mechanism is needed. This is assumed to happen by an extraneous agent, such as heat-induced drying, absorption on mineral surface, or restraining within lipid vesicles or mineral pores. LF has a built-in concentration mechanism, based on the hydrophobic interactions among tails, which bring the headgroups together.

4. (iv) 

   Heat stability: In RF, the biopolymers are heat labile, in terms of both polymer covalent integrity and three-dimensional structure (Shapiro, 2000). In LF, amphiphile assemblies are considerably more heat stable, with hydrophobic interactions augmented with increasing temperature.

5. (v)

   Information content: For replication/reproduction, information has to be stored and transmitted across generations. The sequence-based information in RF is considerably more effective and has the advantage of being copied through a base-pairing mechanism. In LF, compositional information, although less efficient, is still stored and transmitted upon assembly growth-fission cycles. While there is an admitted paucity of experimental data to directly back such a scenario, supporting data are beginning to accumulate (Bukhryakov et al., 2015), and it is hard to miss the analogy of compositional reproduction to epigenetic inheritance (Pulselli et al., 2009), a cornerstone of information transfer in nowadays living cells (Dupont et al., 2009).

6. (vi)

    Catalysis: In parallel to free energy source, this is a fundamental requirement for a lifelike entity to sustain itself away from equilibrium. Enhanced catalytic capacities are also crucial for transiting from a “naked replicator” to a protocell endowed with metabolism and genetic encoding. Regarding RF, there is a large body of experimental evidence for RNA being catalytic, including rate enhancement of biopolymer formation and of metabolism-like reactions. For LF, direct evidence is less abundant, but as amphiphiles are flexible in headgroup choice, amino acids or peptides may play this role, conferring catalytic properties (Zhang, 2012). In addition, micelles may act catalytically to make more amphiphiles as experimentally documented (Bachmann et al., ; Bissette et al., ; Post et al., 2018). Catalysis is facilitated by restriction to 2-D diffusion (reduced dimensionality [McCloskey and Poo, 1986]) and by curvature-induced free energy gradients (Seifert, 1993). Lipid assemblies have also been experimentally shown to harbor rudimentary mutually catalytic networks, with a capacity for replication-like behavior (Bukhryakov et al., ; Hardy et al., 2015).