Abstract
How life arose on the primitive Earth is one of the biggest questions in science. Biomolecular emergence scenarios have proliferated in the literature but accounting for the ubiquity of oxidized (+ 5) phosphate (PO43−) in extant biochemistries has been challenging due to the dearth of phosphate and molecular oxygen on the primordial Earth. A compelling body of work suggests that exogenous schreibersite ((Fe,Ni)3P) was delivered to Earth via meteorite impacts during the Heavy Bombardment (ca. 4.1–3.8 Gya) and there converted to reduced P oxyanions (e.g., phosphite (HPO32−) and hypophosphite (H2PO2−)) and phosphonates. Inspired by this idea, we review the relevant literature to deduce a plausible reduced phospholipid analog of modern phosphatidylcholines that could have emerged in a primordial hydrothermal setting. A shallow alkaline lacustrine basin underlain by active hydrothermal fissures and meteoritic schreibersite-, clay-, and metal-enriched sediments is envisioned. The water column is laden with known and putative primordial hydrothermal reagents. Small system dimensions and thermal- and UV-driven evaporation further concentrate chemical precursors. We hypothesize that a reduced phospholipid arises from Fischer–Tropsch-type (FTT) production of a C8 alkanoic acid, which condenses with an organophosphinate (derived from schreibersite corrosion to hypophosphite with subsequent methylation/oxidation), to yield a reduced protophospholipid. This then condenses with an α-amino nitrile (derived from Strecker-type reactions) to form the polar head. Preliminary modeling results indicate that reduced phospholipids do not aggregate rapidly; however, single layer micelles are stable up to aggregates with approximately 100 molecules.
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Introduction
Phosphorus (P) is one of the most crucial elements for life, which has inspired a prodigious body of literature accumulated over the last half century. P is one of the most versatile of the elements, able to assume an impressive range of oxidation and coordination states that account for its participation in myriad biotic and abiotic chemical reactions. However, owing to Earth’s strongly oxidizing atmosphere since the Great Oxidation Event (ca. 2.3 Gya), it is the highly oxidized (+ 5) phosphate (PO43−) that has evolved to be the dominant P form constituting the metabolic, informational, and structural systems of contemporary life (Arrhenius et al. 1997; Bowler et al. 2010; Hanrahan et al. 2005; Keefe and Miller 1995; Miller 1953; Morton and Edwards 2005; Pasek 2008; Pasek and Kee 2011; Schwartz 1971, 1972, 1997, 2006; Todd 1959; Westheimer 1987). The ubiquity of phosphate P in biochemical systems is rooted in its unique thermodynamic instability and kinetic stability, resonance stabilization, buffering capacities, and nearly constant oxidation state under the redox conditions of the modern atmosphere. These special properties facilitate formation of biologically important compounds containing P-O-C, P–C, and P-O-P linkages that are facilely assembled and degraded enzymatically in support of the chemical demands of living systems (Arrhenius et al. 1997; Bowler et al. 2010; Cooper et al. 1992; de Graaf et al. 1995, 1997, 1998; Gulick 1955, 1957; Hanrahan et al. 2005; Jones and Lipmann 1960; Kee 2013; Pasek 2008; Pasek et al. 2015, 2008; Pasek and Kee 2011; Pech 2011; Peyser and Ferris 2001; Pirim et al. 2014; Robertson and Joyce 2012; Schwartz 1971, 1972, 1997, 2006; Todd 1959; Westheimer 1987). The P–C linkages that define phosphonates have received special attention because, in contrast to P-O-C linkages, they do not readily undergo hydrolytic, thermal, or UV decomposition. Such robust properties may account for the abundance of phosphonates in marine systems, which may be a relic of their greater abundance and importance on the primitive Earth at the origins of life (Pasek 2008). Indeed, the remarkable nature of P was perhaps most eloquently articulated by Nobel Laureate Sir Alexander Todd in his famous musing: “Where there’s life, there’s phosphorus,” which has since been immortalized in the P biochemistry community as “Todd’s Hypothesis” (Todd 1959).
A paradox of the profound importance of P to biological systems is that nearly all terrestrial P has been locked up in unreactive mineral forms (e.g., apatites [Ca5(PO4)3(OH,F,Cl)]) throughout Earth’s history (the “phosphate problem”). As a result, P limits biological productivity on a global scale (Gulick 1955, 1957; Gull 2014; Keefe and Miller 1995; Morton and Edwards 2005; Pasek 2008; Pasek et al. 2015, 2008; Pasek and Kee 2011; Pirim et al. 2014; Schwartz 1971, 1972, 1997, 2006; Todd 1959). When considering this geochemical problem along with a putative partial reducing to mildly oxidizing prebiotic atmosphere, it is difficult to imagine fluxes of terrestrial phosphate P sufficient to supply emergent life chemistries (Chyba and Sagan 1992; Cleaves et al. 2008; Haldane 1929; Hill and Nuth 2003; Joyce 1989; Kasting 1993; Miller 1953, 1955, 1957a, 1957b; Miller and Cleaves 2006; Miller and Urey 1959; Miller et al. 1976; Oparin 1924; Shaw 2008; Walker 1985; Zahnle et al. 2010). A persistent question for the origins of life community has thus been how early life forms could have emerged and utilized such biologically inaccessible forms of P.
Ignited by seminal contributions to this field (Beck et al. 1967; Fox 1973; Gulick 1955, 1957; Haldane 1929; Hargreaves et al. 1977; Jones and Lipmann 1960; Lohrmann and Orgel 1968, 1971, 1973; Miller 1953, 1955, 1957a, 1957b; Miller and Urey 1959; Miller et al. 1976; Oparin 1924; Oparin et al. 1976; Ponnamperuma and Mack 1965; Rabinowitz et al. 1968; Schwartz 1971, 1972; Schwartz and Ponnamperuma 1968; Todd 1959; Yamagata et al. 1979; Yuen and Kvenvolden 1973), and fueled by more recent reports of e.g., alkyl phosphonic acids in the Murchison meteorite (Cooper et al. 1992; Gorrell et al. 2006) and interstellar medium (Turner et al. 2019), photolytic generation of hypophosphorous acid in Nantan meteorite extracts (Bryant and Kee 2006), and phosphate and pyrophosphate synthesis in interstellar dust and cometary particulates (Oro 1995), many research efforts have focused on deducing plausible pathways by which insoluble/unreactive mineral P forms were ultimately converted to more bioaccessible P forms on the early Earth. Though impressive progress has been made on this problem in the last several decades, these efforts have tended to move along terrestrial versus extraterrestrial lines of inquiry (Apel et al. 2002; Britvin et al. 2015; Deamer and Pashley 1989; Gull 2014; Oro and Berry 1987; Oró et al. 1995; Schwartz 2006). However, a number of workers have sought to meld plausible terrestrial and extraterrestrial scenarios to account for the rise and predominance of phosphate P in modern biochemistry (Britvin et al. 2015; Bryant 2009; Bryant et al. 2010; Bryant and Kee 2006; de Graaf et al. 1995, 1997, 1998; Gull 2014; Kee et al. 2013; Maciá et al. 1997; Pasek 2008; Pasek et al. 2007, 2013, 2015, 2008; Pasek and Lauretta 2005a, 2008). One of the more intriguing ideas to emerge from these imaginative efforts, and the one that has largely inspired this work, invokes meteorite delivery of phosphide minerals (e.g., schreibersite [(Fe,Ni)3P]) to Earth during the Heavy Bombardment era (ca. 4.1–3.8 Gya). Upon weathering, these phosphides were converted to more reactive reduced P oxyacids (e.g., phosphite (HPO32−) and hypophosphite (H2PO2−)) and phosphonates within post-Hadean aquatic systems (Bryant, 2013; Bryant and Kee 2006; de Graaf et al. 1995, 1997, 1998; Gorrell et al. 2006; Gull 2014; Hess et al. 2021; Kee et al. 2013; Maciá et al. 1997; Pasek 2008; Pasek et al. 2007, 2013, 2015, 2008; Pasek and Lauretta 2005a; Pirim et al. 2014; Ritson et al. 2020). This idea, and that of a significant role for reduced P in the emergence of life more generally, though still debated (especially in light of reports of terrestrial phosphide deposits (Britvin et al. 2015; Britvin, 2019)), is supported by a growing body of evidence, including but not limited to:
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The majority of late-accreted meteorite impactors are enriched in schreibersite (Catling and Zahnle 2020; Dauphas 2017; Pasek and Lauretta 2008; Ritson et al. 2020).
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Conversion of Fe3P to PO43−, P2O74−, P2O64−, H2PO2−, and HPO32− under mixed atmospheres relevant to primordial Earth (Pasek and Lauretta 2005b).
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Conversion of schreibersite to phosphite, hypophosphorus acid, phosphonates, orthophosphate, hypophosphate, pyrophosphate, triphosphate, and glycerol phosphate (a constituent of modern cell membranes) under mild conditions (Bryant et al. 2013; Bryant and Kee 2006; Pasek et al. 2007, 2013, 2015, 2008; Pasek and Lauretta 2005a).
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Phosphorylation of nucleosides by schreibersite under mild alkaline conditions (Gull et al. 2015).
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Conversion of schreibersite to peroxyphosphates (e.g., HPO52−, HP2O83−) in the presence of H2O2 via Fenton reactions (Pasek 2008; Pasek et al. 2007).
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Production of phosphate (PO43−) and phosphine (PH3) from reduced phosphite and hypophosphite species via disproportionation reactions (Pasek et al. 2014).
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Conversion of schreibersite to phosphine (PH3) (Herschy 2013) in acid media (Pasek et al. 2015).
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Conversion of synthetic schreibersite analogs (e.g., Fe3P) to P oxyanions under mild conditions (Pirim et al. 2014).
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Conversion of phosphite to hypophosphate under mild conditions (Schwartz and van der Veen 1973).
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Conversion of nucleosides to nucleoside-5’-phosphite monoesters via reaction with ammonium phosphite ((NH4)2HPO3)) – a putative primordial constituent – under mild conditions (de Graaf and Schwartz 2005).
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Conversion of interstellar phosphaalkynes to hypophosphorus acid under putative primordial conditions (Gorrell et al. 2006).
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Conversion of mineralized orthophosphate to phosphite under simulated primordial atmospheric spark discharge conditions (de Graaf and Schwartz 2000; Glindemann et al. 1999).
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Reaction of hypophosphorous acid with pyruvate to form amide bonds and pyrophosporous compounds under mild conditions (Bryant et al. 2010).
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Reaction of acetate with schreibersite to form acetylated phosphonates and phosphates, and other compounds containing C-O-P linkages (Pasek et al. 2007).
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Detection of phosphine (PH3) in the atmosphere, sediments, and soils (Eismann et al. 1997; Geng et al. 2005; Glindemann et al. 2003).
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Detection of reduced P in rocks (Herschy, 2018; Pasek, 2020), Archaean marine sediments (Pasek et al. 2013), geothermal pools (Pech et al. 2009), and insect guts (Pech et al. 2011).
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Generation of PO43− from reduced P via photolytic reactions involving reduced sulfur species (Ritson et al. 2020).
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Detection of natural phosphonate estimated to comprise some 25% of total dissolved oceanic P (Clark et al. 1998; Hilderbrand 1983; Kolowith et al. 2001) and some 5% of total soil organic P (Cade-Menun et al. 2002).
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Detection of phosphine (PH3) in the atmospheres of Earth (hypothesized to be a byproduct of anaerobic metabolisms Devai et al. 1988; Glindemann et al. 1996)), Venus (hypothesized as a biosignature (Greaves et al. 2020)), and Jupiter (Fletcher et al. 2009; Irwin et al. 2004; Larson et al. 1977; Prinn and Lewis 1975).
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Detection of methyl phosphine (CH5P) in volcanic gases (Wahrenberger 1997).
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Identification of prokaryotes and lower eukaryotes capable of metabolic utilization of reduced P (Dyhrman et al. 2006; Horiguchi and Kandatstu 1959; Karl 2014; Kittredge et al. 1962; Kononova and Nesmeyanova 2002; Schink and Friedrich 2000; Schink et al. 2002; Stone and White 2012; White and Metcalf 2007; Yang and Metcalf 2004).
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Genomic confirmation of reduced P oxidation to phosphate by the bacterial strain Pseudomonas stutzeri WM88 (Metcalf and Wolfe 1998).
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Detection of fulgurites – peculiar reduced P-containing glassy materials formed via lightening impacts in soils (Hess et al. 2021; Pasek and Block 2009; Pasek et al. 2012).
It seems reasonable to assume then that both meteorite- and electric discharge-associated reduced P would have been supplied in some abundance to primordial hydrothermal systems during the Hadean eon (Bryant et al. 2013; Gorrell et al. 2006; Gulick 1955, 1957; Holm and Baltscheffsky 2011; Holm et al. 2006; Ingmanson 1997; Pasek 2008; Pasek and Block 2009; Pasek et al. 2012, 2013, 2015; Pasek and Lauretta 2005a, 2008; Schoonen and Xu 2001; Schwartz 2006). There, it would have undergone conversion to more reactive P oxyacids and their phosphonate derivatives able to participate in mineral (e.g., phyllosilicate and metal oxide)-catalyzed prebiotic reactions with a variety of known and putative primordial hydrothermal species (e.g., H2, CH4, CO, HCOH, CH3OH, HCOOH, (COOH)2, alkanes, NO3−, NO2−, HCN, NH3, Fe2+, and Fe3+). It follows that such chemistries could also spawn reduced P amphiphiles able to self-assemble into micelles and ultimately more complex membranous structures. These could then sequester and concentrate other prebiotic reactants towards emergence of self-replicating protocellular structures (Bryant and Kee 2006; Deamer 1985, 2004; Deamer et al. 2002; Hazen 2006; Hazen and Sverjensky 2010; Holm and Baltscheffsky 2011; Holm et al. 2006; Maciá et al. 1997; Pasek et al. 2007, 2013, 2015; Pasek and Lauretta 2005a, 2008; Schoonen and Xu 2001). But the question of how such reduced P amphiphiles could emerge from a prebiotic geochemical milieu and assemble into more complex/organized structures along the way to the origins of life remains an open question. To address this problem, varied plausible routes to lipid synthesis in astrobiologically interesting environments have been considered and reported on including, but certainly not limited to, Fischer–Tropsch-type (FTT) reactions in hydrothermal environments (Deamer et al. 2006; Hennet et al. 1992; Holm et al. 2006; Martin et al. 2008; Martin and Russell 2003, 2007; McCollom and Seewald 2007; Shields and Kasting 2007), carbonaceous meteorite and cometary parent bodies, and within circumstellar and interstellar environments (see Oro 1995 for a review).
In surveying this expansive body of work, it seems reasonable to assume that phosphate P likely originated from a synergy of terrestrial and extraterrestrial chemistries. Inspired by this problem and the creative solutions presented to address it over the last several decades, we survey the literature relevant to planetary bioemergence scenarios to present a plausible FTT-based geosynthetic pathway by which a reduced phospholipid analog of present-day phosphatidylcholines could have emerged and evolved towards self-assembly within a primordial volcanic hydrothermal system. The system is presented and contextualized via comparison to putative primordial and extant terrestrial surface (i.e., subaerial) hydrothermal systems.
Constraining the Geophysicochemical Setting
The literature reveals recurring invocation of known and putative primordial synthesis pathways to devise rational prebiotic biomolecular emergence scenarios (Deamer et al. 2002; Gulick 1955; Gulick 1957; Haldane 1929; Miller 1953; Miller 1955; Miller 1957a; Miller 1957b; Miller 1986; Miller and Urey 1959; Miller et al. 1976; Nakatani et al. 2012; Oparin 1924; Orgel 2004; Pasek et al. 2015; Pasek and Lauretta 2005a; Pasek and Lauretta 2008; Saladino et al. 2012; Schwartz 1971; Schwartz 1972; Schwartz 1997; Schwartz 2006; Stüeken, 2013; Wächtershäuser 1988). Accordingly, we assume an extensively meteorite-impacted, tectonically dynamic surface terrain and a relatively shallow hydrothermal lacustrine-type basin system therein, in which chemical constituents can be sufficiently concentrated to overcome the thermodynamic and kinetic barriers associated with more dilute oceanic bioemergence scenarios (Bland and Artemieva 2006; Cockell 2006; Schwartz 2006). We envision this system arising from local volcanic and tectonic activity along a dynamic emergent coastal subduction zone that has undergone extensive meteorite bombardment over a time period on the order of thousands to hundreds of thousands of years. We imagine that smaller mass meteorites impacting the system would have delivered a significant schreibersite inventory to the basin and to the adjoining surface environments (terrestrial and aquatic) over this time frame. We further consider that larger schreibersite-enriched impactors (e.g., enstatites and achondrites) influenced the geology and chemistries of the larger region which, once cooled and submerged by the rising waters of an embryonic primordial coastal ocean, would concentrate reduced P species (via aqueous corrosion of schreibersite) and distribute them to the basin via subsurface hydrological regimes. Figure 1 shows an artist’s rendition of the larger primordial landscape in which we envision the reduced phospholipid assembling and evolving towards self-assembly and plausible biofunctionality. Within this larger geological system, we propose that a smaller area/volume basin (as e.g., that depicted in the lower right of Fig. 1) would likely be the most amenable to driving the chemistries needed to yield the proposed reduced phospholipid. We imagine this smaller inland basin to be defined by system dimensions conducive to the strong evaporative force needed to overcome the thermodynamic constraints on e.g., aqueous condensation reactions. The reasonableness of such a lacustrine-type hydrothermal catchment setting is supported by a number of recent investigations of extant alkaline subaerial hot spring systems relevant to origins of life studies in e.g., North America, Russia, India, New Zealand, and Australia (Damer and Deamer 2020; Deamer 2021; Deamer et al. 2006; Des Marais and Walter 2019; Djokic et al. 2020, 2017; Kompanichenko 2013, 2019; Kompanichenko et al. 2015; Pirajno and van Kranendonk 2005).
Thermal and pH regimes within the proposed setting are selected to encompass the range of extant and putative primordial subaerial hydrothermal parameters reported in the literature that should generate the favorable thermodynamic and kinetic conditions needed to drive the proposed chemistries. Our selection of these regimes is informed by 1) estimates of mean global temperature at the putative origins of life on Earth in the range of 55 to 85 °C, consistent with those of a number of studied volcanic terrestrial hot springs (Knauth and Lowe 2003); 2) the need for higher temperatures (e.g., in the range of 70 to 100 °C surface and ~ 200 °C in subsurface water-steam environments) to overcome activation energy barriers to dehydration synthesis reactions (Damer and Deamer 2020; Deamer 2021; Des Marais and Walter 2019; Joshi et al. 2021; Kompanichenko 2013; Kompanichenko et al. 2015; Milshteyn et al. 2018); 3) reports of typical hydrothermal fluid temperatures in the range of ambient to 100 °C (Djokic et al. 2020; Sojo et al. 2016); and 4) the need for elevated temperature and pH regimes conducive to evaporative forcing to drive e.g., acid dissociation and dehydration synthesis reactions towards the molecular complexity requisite for bioemergence (Damer and Deamer 2020; Deamer 2021; Des Marais and Walter 2019; Djokic et al. 2020, 2017). To provide additional perspective, extant analog systems that have inspired the proposed setting include e.g., Palette Spring and Bison Pool in Yellowstone National Park, USA; the hot springs of the Ladakh region of Northern India; the siliceous sinter zones within the Champagne Pool hot springs of the Rotorua, New Zealand region; and the Kuldur and Mutnovsky hydrothermal systems of the Russian far east (adjoining the Kamchatka Peninsula) and Kamchatka Peninsula, respectively (Deamer 2021; Des Marais and Walter 2019; Kompanichenko 2017; Kompanichenko et al. 2015; Milshteyn et al. 2018; Pandey, 2020). The extinct Dresser Formation of Pilbara Craton, Western Australia provides additional perspective as a well characterized paleo-analog hydrothermal system that dates back to the putative period of life’s emergence on Earth some 3.5 Ga (Djokic et al. 2020, 2017; Pirajno and van Kranendonk 2005; Van Kranendonk et al. 2021).
We further assume a near-surface atmosphere of putative mixed redox regimes derived from impactor and tectonic degassing and subsequent photolysis (Benner et al. 2020). To fine tune the system towards more chemically productive peripheral and sub-surface microenvironments characterized by richer assemblages of organic and mineral constituents, and the steeper physicochemical gradients needed to drive endergonic reactions (McCollom and Seewald 2007), a hydrothermal lacustrine-type basin with the following general characteristics is proposed:
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Small/shallow (ca. 100 m2/5 m), tectonically active basin to assure reactive concentrations (high mirco- to low milli-molar) of organic and mineral constituents (Cleaves II 2013; Cleaves II et al. 2012; Damer and Deamer 2020; Deamer 2021; Deamer et al. 2019, 2006; Deamer and Georgiou 2015; Hennet et al. 1992; Holm et al. 2006; Ingmanson 1997; McKay 1991; Milshteyn et al. 2018).
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Sufficient density of organic and inorganic particulates in the water column for attenuation of destructive UV penetration at depths (Tedetti and Sempéré 2006).
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Thermal (ca. 200 °C/30 °C bottom/surface layers)- and pH (ca. pH ~ 12/pH ~ 6 bottom/surface layers)-stratified water column yielding mixed median layers on the order of 70–90 °C and pH ~ 8–9, respectively. Hotter waters in the benthos (i.e., at the water–sediment/-rock interfaces) would ensure favorable reaction thermodynamics and kinetics to facilitate FTT chemistries (Deamer et al. 2006; Hennet et al. 1992; Holm et al. 2006; Martin et al. 2008; Martin and Russell 2003, 2006; McCollom and Seewald 2007; Shields and Kasting 2007).
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Thermal- and UV-driven evaporation cycles to concentrate solutes along the periphery of the basin to increase molecular collision frequencies and drive essential dehydration synthesis reactions on catalytic mineral surfaces (Cockell 2006; Damer and Deamer 2015, 2020; Deamer 2021; Deamer et al. 2019, 2006; Deamer and Georgiou 2015; Milshteyn et al. 2018; Pascal and Boiteau 2011; Pascal et al. 2013).
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Water column underlain by hydrothermal fissures atop a dynamic crustal subduction region covered by particulate meteoritic schreibersite-, clay-, and iron-enriched sediments (Holm and Baltscheffsky 2011; Holm et al. 2006; Ingmanson 1997).
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Enrichment of the water with mineral particulates derived from meteoritic deposition to catalyze reactions at the particle-water interface (Rotelli et al. 2016; Saladino et al. 2013, 2018, 2011).
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Subsurface intrusion of cooler (~ 25 °C) waters derived from surface runoff/seepage into bottom layers to establish thermal gradients for driving FTT conversion of CO2, CO, H2O, and H2 to hydrocarbons and oxyhydrocarbons (e.g., alkanes, alkanoic acids, alkanols, and ketones) (Martin and Russell 2003; Shock and Schulte 1998)) and metal nitride (e.g., FexN)-catalyzed ammonia production and Strecker-type syntheses of amino nitriles (Hennet et al. 1992; Holm et al. 2006; Shock and Schulte 1998; Smirnov et al. 2008; Summers 1999; Summers and Chang 1993).
Such a proposed geophysicochemical system/setting is analogous to extant hydrothermal systems and consistent with those putative primordial systems existing far from equilibrium, as would be required for non-enzymatic biomolecular emergence (Arrhenius et al. 1997; Bernstein 2006; Bishop et al. 1972; Cleaves II 2013; Cody 2004; Damer and Deamer 2020; Deamer 2021; Deamer et al. 2006; Des Marais and Walter 2019; Djokic et al. 2020; Holm 1992; Holm and Andersson 2005; Holm and Baltscheffsky 2011; Holm and Charlou 2001; Holm et al. 2006; Ingmanson 1997; Kompanichenko 2019; Kompanichenko et al. 2015; Krishnamurthy et al. 1999; Martin et al. 2008; Martin and Russell 2003; Martin and Russell 2006; McCollom et al. 1999; McCollom and Seewald 2007; Miller and Lazcano 1995; Nisbet and Sleep 2001; Ruiz-Mirazo et al. 2014; Rushdi and Simoneit 2001; Schoonen et al. 2004; Schoonen and Xu 2001; Simoneit 2004; Stüeken et al. 2013; Wächtershäuser 1988; Yamagata et al. 1991). Figure 2 shows a more detailed, finer scale depiction of the volcanically/tectonically impacted geophysicochemical processes at work within the smaller inland hydrothermal water body illustrated in the foreground of Fig. 1.
As noted above, we assume a near-surface atmosphere with sharp redox gradients predominated by dynamic fluxes of NH3, CH4, CO2, CO, N2, and H2O, along with volcanic and hydrothermal particulate loadings and strong but variable solar UV flux from the faint young sun. We assume that several of these gases (CO2 and H2O in particular) operate in synergy with particulates to attenuate biologically antagonistic UV (Kasting et al. 1989; Ranjan and Sasselov 2016; Rontó et al. 2003; Wilkinson and Johnston 1950; Wolf and Toon 2010). Injections of volcanic sulfur species (e.g., SO2 and H2S that photolytically decompose to sulfur vapor (S8)) and aldehydes (e.g., acetaldehyde), as well as photolytic formation of organic hazes, further attenuate UV (Kasting et al. 1989; Sagan 1973; Sagan and Chyba 1997). Surface microlayers within the basin proposed above would reduce damaging UV flux to the water column by concentrating UV-absorbing polymers and particulate/dissolved organic matter derived from water column mixing, wet/dry deposition, and terrestrial weathering/runoff (Galgani and Engel 2016; Sagan 1973). UV-absorbing HCN-derived polymers, along with purines and pyrimidines, in the basin would also provide some UV protection for hydrous reactions (Basile et al. 1984; Cleaves and Miller 1998; Sagan 1973). Day-night cycles would have provided additional UV protections by permitting reactions not favored under harsher daytime radiation regimes to occur at night via e.g., residual heat from irradiated rocks and physicochemical gradients at hydrothermal fissures/vents (Spitzer et al. 2015).
Upon cessation of intensive meteorite impacts, hot chondritic materials and impact-modified surface minerals would have released a complex inventory of reduced gaseous species (e.g., CH4, CO, H2, N2, NH3, etc.) to generate near-surface partial reducing conditions (Hashimoto et al. 2007; Kasting 1990; Kasting 1993; Miller 1953; Miller 1955; Miller 1957a; Miller 1957b; Miller 1986; Miller and Urey 1959; Miller et al. 1976; Powner and Sutherland 2011; Schaefer and Fegley Jr 2007; Schaefer and Fegley Jr 2010; Zahnle et al. 2010). Subsequent cooling, condensation, and wet/dry deposition to the surface microlayer of the water body could then concentrate reactants in the system (Cleaves et al. 2008; Donaldson et al. 2004; Griffith et al. 2012; Miller 1953; Miller 1955; Miller 1957a; Miller 1957b; Miller 1986; Miller and Cleaves 2006; Miller and Urey 1959; Miller et al. 1976; Pasek and Lauretta 2008; Stüeken et al. 2013; Tuck 2002; Yuen et al. 1981). These same processes would have generated a number of other important prebiotic precursors, e.g., C2H2, C2H4, S2, CS, CS2, COS, CO2, HCN, and NO2−/NO3− (which could, in addition to driving prebiotic reactions, also attenuate destructive UV photons). Support for this is provided by spectroscopic observations of large-scale impact emissions associated with the Comet Shoemaker-Levy 9 collisions with Jupiter (Harrington et al. 2004). Though Jovian atmospheric and surface environments are clearly distinct from those of Earth, similar primordial scenarios have been invoked to account for biomolecular emergence. It is thus reasonable to presume that such conditions were likely typical of at least some fraction of Earth’s post-Heavy Bombardment era (Abramov and Mojzsis 2009; Mukhin 2010; Valley et al. 2002).
A steady flux of meteorites and dust to Earth during this period would have also delivered copious C-, O-, H-, N-, and P-containing species to seed the proposed system with critical masses of prebiotic reagents (Anders 1989; Bernstein 2006; Brownlee et al. 2006; Chyba and Sagan 1992; Chyba et al. 1990; Cooper et al. 2011, 1992; Cronin and Chang 1993; Cronin et al. 1988; Deamer 1985; Deamer et al. 2002; Deamer and Pashley 1989; Ehrenfreund, 2002; Flynn et al. 2004; Gulick 1955, 1957; Hill and Nuth 2003; Keil 1969; Oro and Berry 1987; Oró et al. 1995). In support of this, time-integrated estimates of extraterrestrial organic matter inputs to the primordial atmosphere are on the order of 1010 kg yr−1 (Chyba and Sagan 1992). More recent measurements of sub-millimeter size interplanetary dust particles impacting the upper atmosphere indicate that on the order of 107 kg yr−1 of extraterrestrial dust enters Earth’s atmosphere (Love and Brownlee 1993). As primordial surface environments cooled to temperatures supportive of stable atmosphere and ocean formation, such interplanetary chemical fluxes would have contributed to chemistries conducive to the emergence of biochemically useful compounds within the primordial atmosphere (Cleaves et al. 2008; Miller 1953; Miller 1955; Miller 1957a; Miller 1957b; Miller 1986; Miller and Cleaves 2006; Miller and Urey 1959; Miller et al. 1976; Pasek and Lauretta 2008). Deposition and subsequent concentration on surface and sub-surface mineral phases thereafter would have permitted the solid, liquid, and gas phase disequilibria needed for prebiotic self-assembly and self-replication of amphiphiles (Apel et al. 2002; Brasier et al. 2011; Bryant et al. 2009; Cleaves II et al. 2012; Groen et al. 2012; Hashimoto et al. 2007; Hinman 2013; Papineau 2010; Pascal and Boiteau 2011; Pasek et al. 2015; Schaefer and Fegley Jr 2007; Schaefer and Fegley Jr 2010; Schoonen et al. 2004; Sleep 2010; Wächtershäuser 1988).
The notion of extraterrestrial delivery of schreibersite ((Fe,Ni)3P) continues to gain broad acceptance as a likely mechanism by which reactive forms of reduced P were supplied to primordial environments that eventually gave rise to phosphate-dominated biochemistries (Gulick 1955, 1957; Keil 1969; Pasek 2006, 2008; Pasek et al. 2007, 2015, 2014; Pasek and Lauretta 2005a, 2008; Ritson et al. 2020; Schwartz 1997, 2006). Some recent debate has also centered on the extent to which other terrestrial and extraterrestrial mineral forms (e.g., whitlockite [Ca18H2(Mg,Fe)2(PO4)14], brushite [Ca[PO3(OH)]·2H2O], apatite [Ca5(PO4)3(OH,F)], and struvite [Mg(NH4)(PO4).6H2O]) may have provided reactive P forms for bimolecular emergence (Arrhenius et al. 1997; Brearley and Jones 1998; Gull and Pasek 2013; Handschuh and Orgel 1973; Hazen, 2008; Weiner and Dove 2003). In addition to the schreibersite-derived reduced P forms discussed (Adcock et al. 2013; Bryant et al. 2009; Bryant et al. 2013; Bryant et al. 2010; Bryant and Kee 2006; Cooper et al. 1992; de Graaf and Schwartz 2000; de Graaf et al. 1995, 1997, 1998; Gorrell et al. 2006; Pasek 2008; Pasek et al. 2007, 2015; Pasek and Lauretta 2005a, 2008), other meteoritic- and electric discharge-associated organic compounds essential for primitive micelle and vesicle formation would have included short chain (i.e., up to about C10) fatty acids (Deamer et al. 2002, 2006; Lawless and Yuen 1979; Oro 1995; Yuen and Kvenvolden 1973) and labile amino (NH2) and nitrile (CN) groups available for incorporation into the polar head groups of emerging amphiphiles (Cleaves II 2010; Lazcano 1986, 2010; Matthews and Minard 2006; Meierhenrich et al. 2004; Miller and Cleaves 2006; Oparin 1924; Pascal et al. 2005). NH3 and HCN in particular have been suggested as probable sources of such polar functional groups on the early Earth, originating from both endogenous and exogenous sources (Cleaves et al. 2008; Cleaves II 2010; Kasting 1993; Miller and Cleaves 2006; Zahnle et al. 2010). With this versatile inventory of reactive species, mineral phases, and thermal and chemical gradients, a plausible geochemical scenario can be envisioned in which a primitive reduced P amphiphile assembles prebiotically in a relatively shallow mineral enriched hydrothermal basin.
Assembly of the Hydrophobic Tail
As noted, hydrothermal systems are frequently invoked settings for exploring plausible routes of prebiotic syntheses leading to origins of life on account of the abundance and diversity of precursor species and the extreme physicochemical gradients (Barge et al. 2015; Baross and Hoffman 1985; Burcar et al. 2015; Cody 2004; Corliss 1981; Damer and Deamer 2020; Deamer and Damer 2017; Deamer et al. 2019; Deamer and Georgiou 2015; Holm 1992; Holm and Baltscheffsky 2011; Holm et al. 2006; Ingmanson 1997; Martin et al. 2008; Martin and Russell 2003, 2006; McCollom et al. 1999; McCollom and Seewald 2007; Nisbet and Sleep 2001; Oparin 1924; Pace 1991; Russell, 2014; Schoonen et al. 2004; Schoonen and Xu 2001; Shock 1990), including those yielding short carbon chain amphiphiles, upon which the proposed reduced phospholipid is based (Deamer et al. 2019; Deamer and Georgiou 2015; Jordan et al. 2019a, 2019b; McCollom et al. 1999; Rushdi and Simoneit 2001). Such species, assuming their accumulation to reasonable (e.g., low millimolar) levels within neutral to alkaline primordial microenvironments (due to e.g., molecular crowding), are generally regarded as well suited for reactions leading to prebiotic micelle and vesicle formation (Apel et al. 2002; Budin and Szostak 2011; Cape et al. 2011; Deamer 1985; Deamer and Pashley 1989; Groen et al. 2012; Monnard and Deamer 2003; Sephton 2002; Spitzer 2013; Spitzer et al. 2015; Zhu and Szostak 2009). Thus, to assemble a plausible hydrophobic tail, formation of a C8 alkanoic (octanoic) acid via clay- and Fe-catalyzed FTT synthesis from hydrothermal H2 and CO (derived from e.g., serpentinization reactions or oxalic and formic acid decomposition) is proposed (Bernstein 2006; Deamer et al. 2002; Martin et al. 2008; Martin and Russell 2003, 2006; McCollom et al. 1999; McCollom and Seewald 2007; Nisbet and Sleep 2001; Rushdi and Simoneit 2001; Segré et al. 2001). Though the magnitudes of H2 available for prebiotic chemistries of these types are still debated, a number of studies suggest abundances sufficient for prebiotic assembly of short chain hydrocarbons (Cleaves II 2008; McCollom et al. 1999; McCollom and Seewald 2007; Miller and Cleaves 2006; Nisbet and Sleep 2001; Oro 1995; Powner and Sutherland 2011; Schwartz 2006). Single chain amphiphiles in particular are thought to have been fairly ideal for prebiotic micelle and vesicle formation due to their more favorable water solubilities, solute permeabilities/diffusivities, and formation thermodynamics and kinetics, especially in association with catalytic mineral phases (Apel et al. 2002; Chen and Szostak 2004; Deamer et al. 2019, 2002; Groen et al. 2012; Segré et al. 2001; Stüeken et al. 2013). In support of this, a number of theoretical and synthesized putative prebiotic amphiphiles have been reported, including short chain fatty alcohols, fatty acids, alkyl sulfates, acylglycerols, alkyl phosphates, alkyl ammonium phosphates, polyprenyl phosphates, polycyclic aromatic hydrocarbons, and amines (Apel et al. 2002; Groen et al. 2012; Jordan et al. 2019b; McCollom et al. 1999; McCollom and Seewald 2007; Nakatani et al. 2012, 2014; Powner and Sutherland 2011; Ruiz-Mirazo et al. 2014; Rushdi and Simoneit 2001; Segré et al. 2001; Thomas and Rana 2007). Short chain alkanes have also been reported to predominate in terrestrial hot springs, geochemical systems analogous to that proposed here (Deamer 2021; Deamer et al. 2019; Des Marais and Walter 2019; Kompanichenko et al. 2015; Milshteyn et al. 2018; Van Kranendonk et al. 2021).
FTT chemistries involving CO and H2 are well studied industrial routes for producing short chain hydrocarbons and their oxy derivatives (Holm and Charlou 2001; McCollom et al. 1999; McCollom and Seewald 2007; Rushdi and Simoneit 2001); they are also commonly invoked as putative routes to abiotic formation within meteorites, hydrothermal systems, and interplanetary and interstellar media (McCollom et al. 1999; McCollom and Seewald 2007; Oro 1995; Rushdi and Simoneit 2001; Studier et al. 1972). In primordial hydrothermal environments, decomposition of formaldehyde (HCHO) and small organic acids (e.g., formic (HCOOH) and oxalic (COOH)2) are also thought to have contributed essential precursors for prebiotic assembly via FTT reactions (Holm and Charlou 2001; Holm et al. 2006; McCollom et al. 1999; McCollom and Seewald 2007; Miller and Cleaves 2006; Nisbet and Sleep 2001; Orgel 2004; Ruiz-Bermejo et al. 2011; Ruiz-Mirazo et al. 2014; Rushdi and Simoneit 2001; Shock and Schulte 1998). In support of this, McCollom et al. (McCollom et al. 1999) reported FTT synthesis of lipids from aqueous solutions of formic and oxalic acids (both used as proxies for the production of CO, CO2, and H2) under hydrothermal conditions. There, upon heating to 175 °C, lipid mixtures were produced containing C2 to > C35 n-alkanols, n-alkanoic acids, n-alkanes, n-alkenes, and alkanones. Comparable mixtures of alkane, alkanol, and alkanoic acid products were also detected when oxalic acid was incubated with montmorillonite clay under similar conditions (Mißbach et al. 2018). Synthesis of straight chain fatty acids in the C5 to C20 range has also been reported on catalytic Fe–Ni meteorites (Nooner and Oro 1979).
Volcanic emissions and associated electrical discharges were almost certainly pervasive in the primordial atmosphere (Glindemann et al. 1999; Kasting 1993; Markhinin and Podkletnov 1977; Yamagata et al. 1979, 1981; Yamagata and Mohri 1982; Zolotov and Shock 2000). Thus, additional CO2, CO, H2O, and H2 reservoirs, as well as steep energy gradients, would have been available to drive the formation of alkane and alkanoic acid mixtures in atmospheric and aquatic compartments (Allen and Ponnamperuma 1967; Ruiz-Bermejo et al. 2011; Zolotov and Shock 2000). Within volcanic emissions, the cooler (i.e., < 250 °C) zones of volcanic plumes likely provided more thermodynamically favorable environments for hydrocarbon formation (Zolotov and Shock 2000), which could then be delivered to aquatic environments via wet/dry depositional processes and transformed into oxyhydrocarbons. These plumes would have also provided steep heterogeneous thermal and particulate gradients for maintaining requisite chemical disequilibria. Combined thermodynamic modeling (Zolotov and Shock 2000) and controlled spark discharge experiments (Allen and Ponnamperuma 1967; Ruiz-Bermejo et al. 2011; Yuen et al. 1981) lend support to these ideas.
Further justification for the C8 alkane hydrophobic tail is provided by detection of short chain alkanes in terrestrial hot water springs (Deamer et al. 2019; Kompanichenko et al. 2015) and in Murchison meteorite extracts (Deamer 1985; Deamer and Pashley 1989; Lawless 1980; Lawless and Yuen 1979; Yuen and Kvenvolden 1973). In Murchison extracts, fatty acid and alkyl phosphonic acid (Cooper et al. 1992) abundances decreased dramatically with increasing carbon chain length. C1 to C12 fatty acids were also reported to predominate in extracts of Murray (Australia), Murchison (Australia), and Asuka (Antarctica) meteorites (Lawless and Yuen 1979; Naraoka et al. 1999; Yuen et al. 1984; Yuen and Kvenvolden 1973). Though consensus for a predominantly reducing primordial atmosphere is waning, simulated spark discharge experiments under reducing (e.g., CH4 and N2) atmospheres has also been shown to produce C2 to C7 fatty acids (Yuen et al. 1981). Such findings are important, as it is quite difficult to imagine a primordial atmosphere lacking at least localized reducing compartments, especially in near-surface environments. The available data suggest that abiotic fatty acid formation in model terrestrial hot spring systems and meteorites may be constrained to an upper bound chain length of about C12, with C6 to C10 configurations likely most stable and in the highest concentrations within primordial environments, making them best suited for chemical selection and self-assembly (Apel et al. 2002; Deamer 1985, 2004; Deamer et al. 2019, 2002, 2006; Deamer and Pashley 1989; Hargreaves and Deamer 1978; Hargreaves et al. 1977; Kompanichenko et al. 2015; Lawless 1980; Lawless and Yuen 1979; Monnard and Deamer 2003; Naraoka et al. 1999; Rushdi and Simoneit 2001; Segré et al. 2001; Shimoyama 1997; Yuen et al. 1984, 1981; Yuen and Kvenvolden 1973). Analogous species have also been detected in carbonaceous meteorites (Cronin and Chang 1993; Cronin et al. 1988; Sephton 2005, 2002) and interstellar molecular clouds (Ehrenfreund and Cami 2010; Hollis et al. 2000; Sephton 2005, 2002), providing additional support for their cosmic abundance and probable delivery to and accumulation in early Earth environments.
Assembly of the Hydrophilic Head
To link the octanoic acid to a suitable polar head group functionally analogous to phosphate head groups that dominate modern biochemistry, the following general reaction scenarios are proposed:
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Formation of reactive hypophosphite via UV-catalyzed corrosion of sedimentary meteoritic schreibersite (Pasek 2008; Walling 1975).
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Methylation of hypophosphite via UV and thermal dissociation of short chain primary alkanols (e.g., CH3OH), aldehydes, and ketones to generate alkyl radicals (e.g., •CH3) able to form methylphosphinate (de Graaf et al. 1995, 1997, 1998; McCollom and Seewald 2007; Yang et al. 2012), which then reacts in the presence of UV to form an organophosphinate derivative (e.g., (hydroxymethyl)phosphinate).
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UV- and mineral-catalyzed condensation of the organophosphinate derivative with the C8 alkanoic acid to form the esterified reduced protophospholipid.
In support of the reasonableness of this scenario, schreibersite has been shown to corrode to more reactive orthophosphate (HPO42−), hypophosphate (HP2O63−), and pyrophosphate (HP2O73−) under mild conditions (Bryant and Kee 2006; Pasek et al. 2015; Pasek and Lauretta 2005a). Orthophosphate production is particularly intriguing given its importance in extant biochemistry. Thermodynamic calculations show that, in the presence of H2O2, peroxyphosphates (HPO52− and HP2O83−) can also be generated, but their experimental detection has remained elusive (Bryant and Kee 2006; Gorrell et al. 2006; Pasek 2008; Pasek et al. 2007, 2013, 2015). It is thus difficult at present to infer a plausible role for these species in bioemergent chemistries. Chen and Walde (Chen and Walde 2010) have proposed analogous prebiotic amphiphiles derived from reduced P oxyacids (e.g. n-decylphosphonic acid). de Graaf et al. (de Graaf et al. 1995) have synthesized alkyl phosphonic acids (with highest yields of methylphosphonic acid) detected in the Murchison meteorite via UV irradiation of mixtures of phosphorous acid (H3PO3), primary alcohols, formaldehyde, and sodium phosphite (de Graaf et al. 1995, 1997; Pasek et al. 2007, 2008)). This group also reported UV-catalyzed synthesis of vinyl phosphonic acid from acetylene and sodium phosphite under neutral to mildly basic conditions (de Graaf et al. 1997). Invoking schreibersite as the most plausible source of prebiotic P, and then assuming corrosion to reduced P species demonstrated by others (Pasek 2008, 2017; Pasek et al. 2007; Pasek and Lauretta 2005a), Powner and Sutherland (Powner and Sutherland 2011) generated mixed chain length alkyl ammonium phosphates from mixed chain length (i.e., C2-C10) alkanols with urea ((H2N)2CO) and ammonium phosphate (NH4H2PO4) under relatively mild conditions. Though the abundance of ammonium phosphates on the primordial Earth remains an open question (Ferris and Nicodem 1974; Schwartz 2006; Summers 1999; Summers and Chang 1993), their formation via evaporation of shallow water bodies containing ammonia in contact with lithogenic phosphate minerals seems plausible (Beck et al. 1967; Lohrmann and Orgel 1971). Formation of ammonium phosphates (as the mineral struvite) relevant to prebiotic environments has also been reported (Burcar, 2019; Burcar et al. 2016).
As noted, UV emissions from the faint young sun, though likely quite variable early on, would have probably been antagonistic to the formation of biomolecules in most surface environments. To overcome this, protective microenvironments would have been available within the highly heterogeneous interior spaces of surface minerals and at hospitable water depths in the range of those proposed here (Hart 1978). Lower energy UV photons thought to have driven much of the organic syntheses necessary for the emergence of life prior to ozone evolution (Miller and Urey 1959) could have penetrated to these depths (Hart 1978; Tedetti and Sempéré 2006). Ongoing studies of UV attenuation in water in our lab lend support to this idea (Drummond et al. unpublished data). Volcanic ash and associated mineral ejecta (e.g., pumice) would have attenuated destructive UV while also providing plumes of catalytic aerosols and mineral surfaces upon which additional atmospheric reactions could be catalyzed (Brasier et al. 2011; Cairns-Smith 2005; Cleaves II et al. 2012; Deamer et al. 2002; Hashimoto et al. 2007; Hazen and Sverjensky 2010; Hinman 2013; Markhinin and Podkletnov 1977; Papineau 2010; Schaefer and Fegley Jr 2007; Schaefer and Fegley Jr 2010; Schoonen et al. 2004; Sleep 2010; Stüeken et al. 2013; Wächtershäuser 1988). Products of those reactions would have then been scavenged from the atmosphere via precipitation and/or deposited to surface environments via dry deposition.
To complete assembly of the reduced phospholipid, clay-, Fe-, and UV-catalyzed formation of an α-amino nitrile compound via Strecker-type synthesis from available pools of NH3/NH4+, HCN, HCHO, NO2−/NO3−, and metal nitrides (e.g., FexN) is proposed. Such reagents occur in modern hydrothermal environments, carbonaceous and iron meteorite parent bodies, interplanetary dust particulates, and the interstellar medium, and are thus thought to have been important reactants in primordial hydrothermal systems (Amend and Shock 1998; Bernstein 2006; Burton et al. 2012; Cronin et al. 1988; Ehrenfreund et al. 2002; Hennet et al. 1992; Hill and Nuth 2003; Holm and Andersson 2005; Holm and Baltscheffsky 2011; Holm et al. 2006; Ingmanson 1997; Kasting 1990, 1993; Matthews and Minard 2006; Meierhenrich et al. 2004; Miller 1955, 1957a, 1957b; Miller and Cleaves 2006; Miller and Urey 1959; Nisbet and Sleep 2001; Pizzarello and Cooper 2001; Pizzarello et al. 2003; Saladino et al. 2012; Schoonen et al. 2004; Schoonen and Xu 2001; Schulte and Shock 1995, 1993; Sephton 2005, 2002; Shock 1990, 1992, 1993, 1995; Smirnov et al. 2008; Stribling and Miller 1987; Stüeken et al. 2013). As noted, the proposed chemistries would occur within a relatively small, shallow, alkaline lacustrine system underlain by hydrothermal fissures situated atop and fed by subsurface processes with average water column temperatures in the range of 70–90 °C (deriving from sharp surface-to-bottom thermal gradients and vertical mixing as earlier noted). Solubilized and particulate Fe would provide redox power to drive reduction of H2O to H2. CO2 derived from magmatic intrusions into the lower water column could also be reduced to CO and CH4 under the higher temperature and more diverse mineralogical regimes of the water–sediment/water–rock boundaries (Catling and Zahnle 2020; Zahnle et al. 2020). This could provide more reactive alkyl species (e.g., •CH3) needed to form the proposed phosphonate head group. Additional reducing power (i.e., H2, CH4) would have been provided by serpentinization reactions occurring at depth with subsequent injection of reaction products into the overlying basin with time (Barge, 2014; Deamer et al. 2019; Guzmán-Marmolejo et al. 2013; Russell et al. 2014). Reduction of hydrothermal NO3− and NO2− to NH3/NH4+ in the presence of catalytic FexN compounds could have also driven redox gradients and additional N-containing reagents for sustaining NH3 and HCN production (Baross and Hoffman 1985; Hennet et al. 1992; Holm 1992; Holm and Andersson 2005; Holm and Baltscheffsky 2011; Holm et al. 2006; Holm and Neubeck 2009; Schoonen and Xu 2001; Smirnov et al. 2008; Summers 1999; Summers and Chang 1993).
Thereafter, these constituents could have been concentrated via adsorption/absorption onto/into mineral particulate phases to facilitate reaction thermodynamics and kinetics for nurturing emergent biochemistries (Cleaves II et al. 2012; Hazen and Sverjensky 2010; Hennet et al. 1992; Holm and Baltscheffsky 2011; Holm and Neubeck 2009; Ingmanson 1997; Krishnamurthy et al. 1999; Maciá et al. 1997; Schoonen et al. 2004; Schoonen and Xu 2001; Singireddy et al. 2012; Smirnov et al. 2008). Commensurate tectonic heating associated with localized plate subduction activity could have also injected additional CO2, CO, and CH4 for reaction with NH3 derived from NO3−/NO2− reduction, hydrolysis of reactive nitrides, and N2 reduction via hydrogen sulfide (H2S) and iron-sulfur (e.g., FeS/FeS2) mineral catalysis (Brandes et al. 1998, 2008; Dörr, 2003; Gordon et al. 2013; Holm and Neubeck 2009; Schoonen et al. 2004; Schoonen and Xu 2001; Singireddy et al. 2012; Smirnov et al. 2008; Summers 1999). Photolysis of CH4 and NH3 mixtures above and within the water column, and especially within the organic enriched surface microlayers, could have also contributed additional HCN to drive Strecker-type reactions (Cleaves II 2010; Donaldson et al. 2004; Miller and Cleaves 2006). In support of this idea, HCN availability on the primordial Earth is reasonably inferred from its abundance in the atmospheres of other solar system bodies (e.g., Jupiter and Titan), as well as in comets and in the interstellar medium (Charnley et al. 2002; Ehrenfreund and Cami 2010; Guillemin et al. 2004; Kwok 2016; Martins 2011; Matthews and Minard 2006; Saladino et al. 2012). More general support for the ubiquity of nitrogen organics is found in the reports of urea and amide species in carbonaceous meteorites (Cronin and Chang 1993; Cronin et al. 1988; Sephton 2005, 2002; Shimoyama 1997) and in the interstellar medium (Ehrenfreund and Cami 2010; Remijan, 2014; Sephton 2005, 2002). It is thus reasonable to assume that a sufficient inventory of endogenous and exogenous nitrogen compounds would have been available to participate in prebiotic reactions leading to some configuration of the proposed reduced phospholipid. Figure 3 presents a generalized reaction scheme showing the plausible reaction steps leading to the reduced phospholipid.
Preliminary Assessment of Aggregate Stability
Seeking to understand the potential of the reduced phospholipid to self-assemble and the stability of single layer micelle aggregates, classical molecular dynamics simulations were performed using the GROMACS software package (Abraham et al. 2020). The presence of chiral centers in the reduced phospholipid leads to two enantiomers predicted to be within 0.2 kcal/mol of each other by density functional theory (See Fig. S1 in Supporting Information). The two enantiomers were then studied by performing molecular dynamics simulations containing 50, 100, or 150 reduced phospholipids. The simulations started from initial configurations where the phospholipids were distributed randomly or pre-aggregated into a single layer micelle. In all cases, the concentration of the reduced phospholipid was relatively low at approximately 0.11 mM. A total of 10 ns was simulated in the isobaric ensemble (NPT) for each system (see details in Supporting Information). Simulations of randomly distributed reduced phospholipids show limited aggregation beyond 3–6 phospholipids. This might be attributed to their negative charge hindering the aggregation due to electrostatic repulsion (Figs. 4a and S14-S19 in Supporting Information), which is consistent with their electrostatic potential plot (Fig. S20 in Supporting Information). This limited aggregation could be aided by the presence of additional counterions; however, a slower aggregation would be expected compared with neutral phospholipids. Formation of micelles was not observed within the simulation time scale under the conditions assessed, and our simulations do not indicate a strong tendency of these phospholipids to aggregate here. However, given the nature of the basin envisioned in this work, we expect that the drying cycles would concentrate the phopspholipids into an environment more conducive to aggregation over a longer time span, which would result in improved micelle formation. Simulations of pre-aggregated phospholipids revealed the stability of small and medium micelles with 50 and 100 phospholipids, respectively. On the other hand, large micelles containing 150 phospholipids tend to decrease in nuclearity (Fig. 4b) and, in one case, enantiomer S rapidly evolves into two smaller aggregates (Fig. S7b in the Supporting Information). This indicates that the arbitrarily chosen number of phospholipids in the simulated single layer micelles is not optimal and additional studies are needed to determine that number. Our simulations do agree with recent work (Abdel-Azeim 2020) as the initial spherical micelles evolve into rod like aggregates when CHelpG charges are used (see Supporting Information for videos). Further studies on the formation of micelle structures from single phospholipids, the stability of aggregates at larger time scales, the role of ions, and the effect of the atomic charges on the shape of the phospholipid aggregates are the subject of ongoing studies.
Overall, these simulations support the reasonableness of the proposed reduced phospholipid structure and suggest that it has the requisite properties for self-assembly. These results provide justification for future experimental work aimed at synthesizing the molecule and assessing its potential for self-assembly in vitro under prebiotically relevant conditions.
Conclusions
The chemistry of life demands highly oxidized phosphate P for a stunning array of metabolic, informational, and structural systems. However, virtually all terrestrial P has been locked up in unreactive mineral forms throughout Earth’s history. Couple this with the putative mixed redox states of the primordial atmosphere (that continue to be vigorously debated) and it is difficult to imagine inorganic phosphate reservoirs sufficient to support proliferation of emergent life processes. A key question for the origins of life community has thus been how the earliest life forms were able to utilize such inaccessible P. One intriguing hypothesis invokes extraterrestrial delivery of schreibersite to the early Earth, with subsequent aqueous corrosion to yield reactive reduced P oxyacids and their organic derivatives that may have served as progenitors of the Phosphate World. Inspired by this problem, we hypothesized that these reduced P forms could have combined with a myriad of primordial organic and mineral constituents to form primitive reduced P phospholipid analogs of modern phosphatidylcholines with the potential to self-assemble into primitive membrane structures. Seeking support for this idea, we present a review of the origins literature that has informed our deduction of a prebiotic scenario from which such a primitive phospholipid could have emerged from the putative primordial milieu. The proposed phospholipid assembles in a relatively shallow volcanic alkaline hydrothermal lacustrine-type system underlain by a meteoritic schreibersite-, phyllosilicate-, and iron-enriched benthos. Small system dimensions, coupled with thermal- and UV-driven evaporation cycles, concentrate reactants to increase collision frequencies and overcome thermodynamic and kinetic barriers to emergence and self-assembly. A copious body of literature informs and supports the reasonableness of our proposal and preliminary modeling efforts confirm amphiphilicity and aggregate stability needed for self-assembly.
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Acknowledgements
This work grew out of the first research-based undergraduate Biochemistry and Astrobiology courses taught at Dakota State University (DSU). MOG thanks the DSU leadership for the freedom to redesign these courses to be research-intensive. MOG was supported by the National Science Foundation (NSF)/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and by the South Dakota Board of Regents. MOG and PV were supported by the DSU Faculty Research Initiative (FRI) Grant Program and the DSU College of Arts and Sciences. MOG and PV were further supported by the South Dakota Space Grant Consortium and Southern Oregon University, respectively. The computations supporting this project were performed on High Performance Computing systems at the University of South Dakota funded by the NSF MRI award OAC-1626516. PM, BV, and SKAA were supported by the NSF RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954. PM, BV, and SKAA acknowledge that the land this research was performed on is the original homelands of the Dakota, Lakota, and Nakota tribal nations. PM, BV, and SKAA acknowledge the painful history of genocide and forced removals from this territory, and we honor and respect the many diverse Indigenous peoples still connected to this land on which we gather. PM, BV, and SKAA give thanks for our opportunity to gather on this land to make contributions to science. LMB was supported by the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (NASA). VAS was supported by the Barry M. Goldwater Scholarship and Excellence in Education Foundation. LJL was supported by the DSU Student Research Initiative (SRI) Program. NWF, KLC, and KR were supported by the DSU College of Arts and Sciences. LRD was supported by the DSU SRI Program. LRD and SMD were supported by the NSF/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and by the South Dakota Board of Regents. SG and VK were supported by the Instituto de Astrobiología de Colombia and DSU’s Office of the Provost. We thank Don Dixon of Cosmographica (https://www.cosmographica.com) for enthusiastic permission to reproduce his artwork in support of this research. We thank Dr. Dale Droge (DSU) for many insightful conversations about the manuscript and Nancy Presuhn and Pamela Lewis (DSU) for exceptional administrative support. We are especially grateful to anonymous reviewers for sharing their considerable expertise which has significantly improved the quality and scope of this contribution. We contribute this work in memory of Julian Freitag – a much beloved DSU science student and son of our colleague and friend Dr. Dale Droge – who tragically lost his life during this work.
Funding
MOG was supported by the National Science Foundation/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and the South Dakota Board of Regents, the DSU Faculty Research Initiative (FRI) Grant Program, the DSU College of Arts and Sciences, and the South Dakota Space Grant Consortium. PV was funded by the DSU Faculty Research Initiative (FRI) Grant Program, the DSU College of Arts and Sciences, and with startup funds from Southern Oregon University. PM and BV were supported by the National Science Foundation RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954, and the Department of Chemistry of the University of South Dakota (USD) for start-up funds. SKAA was supported by the National Science Foundation RII Track-2 FEC: Data Driven Material Discovery Center for Bioengineering Innovation award IIA-1920954. LMB was supported by the Jet Propulsion Laboratory, California Institute of Technology, under a contract with the National Aeronautics and Space Administration (NASA). VAS was supported by the Barry M. Goldwater Scholarship and Excellence in Education Foundation. LJL was supported by the DSU Student Research Initiative (SRI) Program. NWF and KLC were supported by the DSU College of Arts and Sciences. KR was supported by the DSU College of Arts and Sciences. LRD was supported by the DSU SRI Program. LRD and SMD were supported by the National Science Foundation/EPSCoR RII Track-1: Building on the 2020 Vision: Expanding Research, Education and Innovation in South Dakota (Award OIA-1849206) and the South Dakota Board of Regents. SG and VK were supported by the Instituto de Astrobiología de Colombia and DSU’s Office of the Provost.
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Gaylor, M.O., Miro, P., Vlaisavljevich, B. et al. Plausible Emergence and Self Assembly of a Primitive Phospholipid from Reduced Phosphorus on the Primordial Earth. Orig Life Evol Biosph 51, 185–213 (2021). https://doi.org/10.1007/s11084-021-09613-4
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DOI: https://doi.org/10.1007/s11084-021-09613-4