Six characters in search of a scenario

1. 1. The first chemical automata most likely emerged in liquid water. According to its molecular weight, water should be a gas under standard terrestrial conditions. Its liquid state is due to its ability to form hydrogen bonds, which also makes water a good solvent. Water is essential in the production of clays and other weathering products of minerals in rock, which would have provided a continual supply of nutrients for life (Westall and Brack, Reference Westall and Brack2018). The earliest environments in which chemical automata developed were locations in which wet−dry cycling conditions prevailed, thereby helping to drive the types of prebiotic chemical reactions required for the emergence of life as we know it (Forsythe et al., Reference Forsythe, Yu, Mamajanov, Grover, Krishnamurthy, Fernández and Hud2015; Becker et al., Reference Becker, Feldmann, Wiedemann, Okamura, Schneider, Iwan, Crisp, Rossa, Amatov and Carell2019; Campbell et al., Reference Campbell, Febrian, McCarthy, Kleinschmidt, Forsythe and Bracher2019; Damer and Deamer, Reference Damer and Deamer2020).

2. 2. It is generally believed that the essential components of primitive chemical automata were organic molecules, i.e., molecules containing carbon and hydrogen atoms associated with oxygen, nitrogen and sulphur atoms, as known in present-day life. With the exception of the small amounts of organic molecules formed in the primitive atmosphere, the majority of carbon molecules on the early Earth were either delivered by carbonaceous chondrites (Pizzarello and Shock, Reference Pizzarello and Shock2010), micrometeorites (Maurette, Reference Maurette2006; Rojas et al., Reference Rojas, Duprat, Engrand, Dartois, Delauche, Godard, Gounelle, Carrillo-Sánchez, Pokorný and Plane2021), and cometary material (Altwegg et al., Reference Altwegg, Balsiger, Bar-Nun, Berthelier, Bieler, Bochsler, Briois, Calmonte, Combi, Cottin, De Keyser, Dhooghe, Fiethe, Fuselier, Gasc, Gombosi, Hansen, Haessig, Jäckel, Kopp, Korth, Le Roy, Mall, Marty, Mousis, Owen, Rème, Rubin, Sémon, Tzou, Hunter Waite and Wurz2016), or formed in the subsurface by processes catalysed by aqueous reactions on the surfaces of subsurface rocks (Martin et al., Reference Martin, Baross, Kelley and Russell2008; Westall et al., Reference Westall, Hickman-Lewis, Hinman, Gautret, Campbell, Bréhéret, Foucher, Hubert, Sorieul, Dass, Kee, Georgelin and Brack2018).

3. 3. Rock and minerals constituting the earliest environments would have played an essential role in the processes that led to the emergence of life (Hazen and Sverjensky, Reference Hazen and Sverjensky2010). Pumice is an example of a rock type that has been promoted as a unique substrate with remarkable potential to support the origin of life (Brasier et al., Reference Brasier, Matthewman, McMahon and Wacey2011). Clays also offer advantageous features as key minerals in origin of life scenarios due to their (1) molecular order and repeating topological arrangement with the ability to serve as polymerization templates, (2) large adsorption capacity with the ability to concentrate organic chemicals, and (3) shielding capacity to protect templated organic molecules against sunlight and other types of incoming radiation (Ertem, Reference Ertem2021). The confinement of several types of organic molecules essential for life in silica gel were likely also necessary for the earliest life (Gorrell et al., Reference Gorrell, Henderson, Albdeery, Savage and Kee2017; Dass et al., Reference Dass, Jaber, Brack, Foucher, Kee, Georgelin and Westall2018).

4. 4. The environmental ‘stage’.

Any plausible model for the origin of life must take into account the geological complexity and diversity of the primitive Earth. Liquid water was present at Earth's surface due to the size of the planet, its distance from the Sun, and the greenhouse atmosphere maintained by crustal recycling as a result of plate tectonics and volcanism that continuously released water and key atmospheric gases important for life, such as CO₂ trapped in subducted carbonates. Other environmental conditions on the ancient Earth were very different from those of today: anoxygenic (Schopf et al., Reference Schopf, Kudryavtsev, Osterhout, Williford, Kitajima, Valley and Sugitani2017), a warm to hot and acidic ocean; a high flux of ultraviolet (UV) radiation (Ranjan and Sasselov, Reference Ranjan and Sasselov2017); and a great amount of volcanic and hydrothermal activity (Nisbet and Sleep, Reference Nisbet and Sleep2001; Westall et al., Reference Westall, Hickman-Lewis, Hinman, Gautret, Campbell, Bréhéret, Foucher, Hubert, Sorieul, Dass, Kee, Georgelin and Brack2018). Accordingly, hydrothermal environments at Earth's surface have gained renewed interest as possible cradles for the origin of life (Sojo et al., Reference Sojo, Herschy, Whicher, Camprubı and Lane2016; Branscomb and Russell, Reference Branscomb and Russell2018; Westall et al., Reference Westall, Hickman-Lewis, Hinman, Gautret, Campbell, Bréhéret, Foucher, Hubert, Sorieul, Dass, Kee, Georgelin and Brack2018; Deamer et al., Reference Deamer, Damer and Kompanichenko2019; Damer and Deamer, Reference Damer and Deamer2020; White et al., Reference White, Shibuya, Vance, Christensen, Bhartia, Kidd, Hoffmann, Stucky, Kanik and Russell2020).

1. 5. Far from equilibrium wet−dry cycling reactants

One can envision a promising area for future research that consists of an open system in which far-from-equilibrium wet−dry cycling of organic reactions occurs repeatedly and iteratively at mineral surfaces under hydrothermal-like conditions. Additional detailed reviews about the origins of cellular life can be found in the literature (Schrum et al., Reference Schrum, Zhu and Szostak2010; Lambert et al., Reference Lambert, Sodupe and Ugliengo2012; Ruiz-Mirazo et al., Reference Ruiz-Mirazo, Briones and de la Escosura2014; Camprubí et al., Reference Camprubí, de Leeuw, House, Raulin, Russell, Spang, Tirumalai and Westall2019).

1. 6. Systems chemistry, the reduction of a problem to a set of essential characteristics, was first used in 2005 by von Kiedrowski (Kindermann et al., Reference Kindermann, Stahl, Reimold, Pankau and von Kiedrowski2005; Stankiewicz and Eckardt, Reference Stankiewicz and Eckardt2006) when describing the kinetic and computational analysis of a nearly exponential organic replicator. As a relevant example of the system chemistry approach, Sutherland's team showed that precursors of ribonucleotides, amino acids and lipids can all be derived by the reductive homologation of hydrogen cyanide and some of its derivatives, and thus that all the cellular subsystems could have arisen simultaneously through common chemistry (Patel et al., Reference Patel, Percivalle, Ritson, Duffy and Sutherland2015). The essence of systems chemistry has also been recently expanded (Strazewski, Reference Strazewski2019).

Two main possible strategies

Two distinct operational approaches, autotrophy and heterotrophy, are promoted as enabling the earliest life, their differences depending upon the role played by CO₂. In the ‘metabolism-first approach,’ the proponents of autotrophic life call for the direct formation of simple molecules from CO₂ to rapidly generate life (Wächtershäuser, Reference Wächtershäuser2007). Energy sources with the capacity to reduce CO₂ were likely provided by the oxidative formation of pyrite from iron sulphide and hydrogen sulphide, which would have given rise to a two-dimensional ‘surface metabolism’. A laboratory test of this scenario in an oceanic setting, as proposed by Michael Russell and colleagues (Martin et al., Reference Martin, Baross, Kelley and Russell2008), simulated the prevailing conditions in alkaline hydrothermal vents and generated low yields of simple organics (Herschy et al., Reference Herschy, Whicher, Camprubi, Watson, Dartnell, Ward, Evans and Lane2014). Hence, a challenge remains for the proponents of a metabolism first approach, namely, to produce large enough precursor prebiotic molecules to support the emergence of life as we know it.

In the second hypothesis, the primeval soup scenario (also known as ‘replication first’), complex organic molecules accumulated in a warm little pond, à la Darwin. Laboratory efforts to generate a primitive living cell-like system with hydrothermal conditions, wet–dry cycling, or minerals continue to the present, with further endeavours required to focus on constraining the boundary conditions to produce key molecules, such as protein enzymes and ribonucleic acid (RNA), and to compartmentalize them (Monnard and Walde, Reference Monnard and Walde2015).

For compartmentalization, amphiphilic compounds can spontaneously assemble into membranous vesicles in hydrothermal fluids (Milshteyn et al., Reference Milshteyn, Damer, Havig and Deamer2018; Damer and Deamer, Reference Damer and Deamer2020). Experiments that demonstrate how different prebiotically available building blocks can become the precursors of vesicle-forming phospholipids were reviewed by Fiore and Strazewski (Reference Fiore and Strazewski2016). For example, mixtures of C10–C15 single-chain amphiphiles form vesicles in aqueous solutions at temperatures of ~70 °C in the presence of isoprenoids and under strongly alkaline conditions (Jordan et al., Reference Jordan, Rammu, Zheludev, Hartley, Maréchal and Lane2019). Vesicles functionalized with RNA and peptides would have provided an interesting step towards the formation of early protocells (Izgu et al., Reference Izgu, Björkbom, Kamat, Lelyveld, Zhang, Jia and Szostak2016).

As for prebiotic peptides, considerations include the role of mineral surface chemistry in controlling their origin (Erastova et al., Reference Erastova, Degiacomi, Fraser and Greenwell2017) and formation on oxide surfaces (Lambert et al., Reference Lambert, Jaber, Georgelin and Stievano2013; Kitadai et al., Reference Kitadai, Oonishi, Umemoto, Usui, Fukushi and Nakashima2017) and on other minerals (Kitadai et al., Reference Kitadai, Nishiuchi and Takahagi2021). The self-assembly of longer prebiotic polypeptides produced by the condensation of non-activated amino acids on oxide surfaces has also been reported (Martra et al., Reference Martra, Deiana, Sakhno, Barberis, Fabbiani, Pazzi and Vincenti2014). Environmentally driven wet–dry cycles would have favoured ester-mediated amide bond formation (Forsythe et al., Reference Forsythe, Yu, Mamajanov, Grover, Krishnamurthy, Fernández and Hud2015), and short peptides were likely to have played a role in the steps that led to the formation of a protocell (Fishkis, Reference Fishkis2007), as reviewed in Frenkel-Pinter et al. (Reference Frenkel-Pinter, Samanta, Ashkenasy and Leman2020).

RNA played probably a starring role in life's emergence (Budin and Szostak, Reference Budin and Szostak2010; Bernhardt, Reference Bernhardt2012; Higgs and Lehman, Reference Higgs and Lehman2015; Benner et al., Reference Benner, Bell, Biondi, Brasser, Carell, Kim, Mojzsis, Omran, Pasek and Trail2020), and significant progress in producing it abiotically in a ‘one-pot synthesis’ has been made. As already mentioned, Sutherland's team has simultaneously produced the precursors of nucleic acid amino acids and lipids, starting with hydrogen cyanide, hydrogen sulphide, and UV light (Patel et al., Reference Patel, Percivalle, Ritson, Duffy and Sutherland2015). The synthesis of the pyrimidine nucleosides driven solely by wet–dry cycles has also been reported (Becker et al., Reference Becker, Feldmann, Wiedemann, Okamura, Schneider, Iwan, Crisp, Rossa, Amatov and Carell2019). In addition, 5′-mono- and diphosphates can form selectively in one-pot reactions in the presence of phosphate-containing minerals. Diamidophosphate efficiently phosphorylates a wide variety of potential building blocks, nucleosides/nucleotides, amino acids, and lipid precursors under aqueous conditions. Significantly, higher-order structures, oligonucleotides, peptides, and liposomes, are formed under the same phosphorylation reaction conditions (Gibard et al., Reference Gibard, Bhowmik, Karki, Kim and Krishnamurthy2018).