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On the Emergence of a Proto-Metabolism and the Assembly of Early Protocells - Elements
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On the Emergence of a Proto-Metabolism and the Assembly of Early Protocells

Protocells are envisaged as encapsulated networks of catalytic polymers, such as RNAs, which are thought to have existed on the prebiotic Earth as precursors to contemporary biological cells. Such protocells were not “alive” in the way this word would apply to a contemporary unicellular organism. Rather, protocells represent a necessary evolutionary step toward those first forms of cellular life. In this review, we explore how chemicals synthesized by minerals or delivered by meteorites could have contributed to the emergence of the first protocells and could have supported these protocell’s evolution towards primitive cellular life.

DOI: 10.2113/gselements.12.6.419

Keywords: protocells, pro metabolism, catalytic mineral surfaces, meteorites, RNA, energetics

Introduction

Whether we will ever unravel how living systems originated on Earth is doubtful. Few pieces of direct evidence for early Earth’s environments, geochemistry, and living systems and/or their precursors exist. Although there is no universally accepted definition of life, researchers in the origin of life field have adopted operative definitions to undertake their investigations. In general, these definitions highlight the central role of water, the ubiquity of cells as basic units of all life forms, and the presence of the triad of DNA/RNA/protein in all life processes. Living systems, even seemingly “simple” prokaryotes, are extremely complex with respect to their molecular components, their structure, and their reaction networks and dynamics.

Moreover, using phylogenomic analysis to surmise the characteristics of early cellular life, one must conclude that even the last universal common ancestor (LUCA) was conceptually not very different from contemporary cells. That is, early cells and the likely systems that preceded them (protocells) were the products of a chemical evolutionary process. Thus, one cannot speak of a protocell type, but rather of a lineage of protocell systems that slowly evolved from simple self-assembled molecular systems towards pre-cellular entities capable of self-sustenance and self-replication.

In their simplest embodiment, inferred from many operative definitions, protocells would have been chemical systems characterized by a compartmentalisation system, a reaction network (even as small as a single reaction) that uses energy transduced from its environment, and some form of information system (Sahai et al. 2016 this issue). The information system should not only be considered as if current biochemistry, but, rather, as a form of information based on the protocell’s chemical composition or its functions, modulated by the physicochemical gradients inherent in its environment. Indeed, even the replication of a sequence-specific polymer sequence (e.g. of an RNA ribozyme) seems to be rather difficult to achieve chemically, a fact that led one pioneer of the field to speak about it as the “biochemist’s dream” (Orgel 2004).

This protocell vision implies that early systems were dependent on the chemicals available in the environment, which were either products of geochemical processes (endogenous syntheses on Earth) or some type of extraterrestrial processes (exogenous syntheses) (Dalai et al. 2016 this issue). Furthermore, in the complex prebiotic milieu, a way to select the chemicals of interest, such as by adsorption on a surface, might have been essential to permit the formation of simple self-assembled systems and their stabilization. As protocell complexity gradually increased, in terms of molecular composition and functions, protocells would have been dependent on external sources of chemical raw materials for constructing their own molecules. Chemical energy from the environment to power a protocell’s reaction pathways would have remained necessary until internal robust energy harvesting processes, possibly based on proteinaceous catalysis, were constructed. All these phases in the development of protocell systems could, therefore, have been supported by mineral surfaces and small mineral particles. This review will focus on protocells, their composition and properties, their emergence, their functions (including chemical and energy uptake mechanisms), and their putative evolution toward early cells. While exploring these themes, possible contributions/involvement of geochemistry and geo-biochemistry will be highlighted.

Protocell Subsystems

A survey of the literature on the design and investigation of protocells highlights significant variety in subject matter and scope, in part due to the rather vague definition of “protocell” and in part due to proposed protocell applications (for medicine, material sciences, and the origin of life). With respect to the origin of life, the expected evolution of protocells (Fig. 1) leads to further multiplication of potentially relevant systems. In their most evolved embodiment, protocells should have been able to independently synthesize their chemicals from simpler chemicals by using energy harvested from the environment (Fig. 2). Even so, it is interesting to define putative functions/properties of the protocell subsystems or component parts.

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Figure 1. General evolution of protocell systems with respect to the relative involvement of geochemistry in protocell self-assembly and function. The thickness of the coloured triangular shapes in the background highlight the trends. (blue) The involvement of geochemistry; (red) The relative complexity of the protocell’s systems.

Compartment

To achieve their autonomy, an essential protocell characteristic would have been compartmentalization, which is the confinement of molecular assemblies within defined boundaries (Monnard and Walde 2015). This process must have been key to their emergence and how they evolved ever-increasing complexity (in terms of molecular composition and related functions), ultimately leading to the phospholipid-based membranes of contemporary biochemistry.

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Figure 2. Schematic representation of an evolved protocell. The environment delivers chemicals, and their precursor molecules, which are used by the protocell to produce its own building blocks. There are two uptake pathways: first, diffusion across the compartment boundaries through transient packing defects (amphiphile molecules continuously move in the compartment boundaries, but not all in the same direction, creating packing defects, or holes in the compartment boundaries); second, direct insertion into the compartment bilayers. The second mechanism is especially relevant for hydrophobic molecules (photosensitizers and amphiphile precursors). Using energy from the environment (light bolt) and the “genetic” information (black arrow), the internal reaction network (the catalysts) converts (red arrows, numbers) the incoming precursor chemicals into new catalysts (I), new information molecules (II), new amphiphiles in the compartment boundaries (III); and new energy harvesting systems (IV), as well as molecules that trigger the self-replication of the whole system (V). The chemicals delivered by the environment are in green letters or their shapes are highlighted in green; new molecules are highlighted with a blue background; the black dash frames indicate the original molecules that are being copied.

The protocell compartment could have had various forms, ranging from inorganic structures to amphiphile structures, as well as mixtures thereof under the express condition that its building blocks could self-assemble due to non-covalent interactions (Monnard and Walde 2015). Protocell composition, nevertheless, had to imperatively evolve towards the lipid-based cell boundaries of contemporary biology. Two other prebiotic compartmentalization properties likely played a central role in determining how protocells functioned: first, stability, both spatial and temporal; second, selective permeability of the compartment boundaries for the exchange of small molecules (Monnard and Walde 2015). These two properties must have been carefully balanced, as too stable a system would not have been able to take up new molecular assemblies necessary for its evolution, while too permeable a boundary would have been an impediment to achieving the necessary local concentration gradients that would allow an internalized catalytic system to produce protocell building blocks efficiently.

Internal Catalytic Network and Information System

The internal catalytic network, often referred to as “metabolism”, is the set of catalysts/catalytic assemblies that a protocell would have required to process resources into its own building blocks (Ruiz-Mirazo et al. 2014). The research on this protocell component has focused on two types of process: (i) the synthesis of biopolymers, and (ii) the synthesis of other protocellular building blocks, most prominently those forming the compartment. Biopolymer synthesis, in particular of RNA due to the RNA-world hypothesis (Mansy and Belmonte 2016 this issue; Maurel and Leclerc 2016 this issue), is considered central to the origin of life due to its ability to catalyze reactions under mild conditions, as well as encode the information necessary to construct a cell. However, catalysis by other “non-genetically” coded molecules—such as metal-ions/complexes (Mansy and Belmonte 2016 this issue), short peptides (Adamala and Szostak 2013), or small mineral particles (Summers and Rodoni 2015)—must have been involved in driving early catalytic networks.

Energy Harvesting

The ability to harvest energy from a primary source (light, heat or chemical energy) and convert it first into chemical bonds and later into chemical energy currencies is a central property of living systems. At first, energy harvesting systems could have been limited to directly converting chemical precursors, present from their environment and activated by abiotic processes, into building blocks or into more complex molecules: that is, performing thermodynamically downhill reactions. The next big evolutionary step would have been the formation of carbon–carbon bonds. Because this bond formation is a two-electron process, it seems likely that this catalytic function would have required some form of chemical gradient. Nevertheless, a simple energy harvesting function would have started an internal catalytic network.

From this short overview of protocell parts, one can directly surmise that protocell development must have been based on a co-emergence and co-evolution of the protocellular parts/functions from an early stage (Caetano-Anollés and Seufferheld 2013; Krishnamurthy 2015). Indeed, only through the interconnection between constituent parts can a functional protocell be realized. Without a compartment, a robust, complex reaction network and information system cannot arise, and energy harvesting will not occur properly. Moreover, the presence of a compartment can promote the functions of the other parts (Monnard and Walde 2015). A compartment cannot be maintained without other protocell parts. These latter parts will not only provide its building blocks, but also define its basic properties (stability and permeability). These observations have resulted in heightened research into the possible significance of chemical systems in the origin of life field, because the development of complex molecular aggregates seem to be consistent with the emergence of cellular complexity. The study of complex molecular aggregates is now called “system chemistry” (Kauffman 2011; Ruiz-Mirazo et al. 2014). The system chemistry approach focuses not so much on chemical diversity or individual chemical reactions, but rather on the potential interactions between chemical reactions or their convergence. Cooperativity within chemical aggregates lies at the heart of system chemistry. Moreover, chemical systems can inherently satisfy the concept of evolutionary continuity.

MOLECULAR COMPOSITION OF PROTOCELL SUBSYSTEMS

The involvement of the geological environment would have been crucial in determining the chemicals that were available and in providing an energy source. Even though the actual composition of chemicals composing early protocells is still not clearly defined, one can infer, both from the likely chemical make-up of the last universal common ancestor and from the analysis of the composition of extraterrestrial chemical sources, which early Earth chemicals would have been available and which chemicals would have had the necessary properties to allow functional protocells to form.

Compartments

A protocell’s original compartment could have formed by mineral formations (Martin and Russell 2003) or by mineral particles (Li et al. 2014), either by concentrating chemicals onto a particular mineral surface or by particle self-assembly, respectively. Among other chemicals, the inventory of carbon compounds in carbonaceous chondrite meteorites has revealed an abundance of fatty acids (molecules with single saturated hydrocarbon chains up to 12 carbons long) but also related chemicals that could serve as chemical precursors for fatty acids (Dalai et al. 2016 this issue).

Models of terrestrial syntheses, such as the Fischer–Tropsch type syntheses, also have the potential to deliver fatty acids, and derivatives, with similar or longer hydrocarbon chain lengths (McCollom et al. 1999). Alkyl phosphates and phosphonates can be synthesized in simple reactions using phosphorus extracted from Fe/Ni–rich meteorites or minerals such as schreibersite (Pasek and Lauretta 2005; Bryant et al 2013). These fatty acid and phosphate-based molecules are amphiphiles and, thus, can spontaneously self-assemble into structures (see Fig. 3) when in aqueous solutions at reasonable temperatures and pressures. Amphiphile vesicles would offer the best conditions for the development of a complex reaction network because they, like cells, can co-localize or compartmentalize molecules in three different micro-environments: 1) in the hydrophobic core of bilayers; 2) at the surface of bilayers; 3) within their aqueous lumen for hydrophilic solutes.

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Figure 3. Energy harvesting systems in amphiphile structures. (A) Decanoic acid, a putative prototypical prebiotic amphiphile. Amphiphiles will only self-assemble into bilayered vesicles (gray circle in centre of image) once their concentration in an aqueous medium surpasses a threshold value, often referred as critical vesicle concentration (CVC). Below the CVC, amphiphiles are present as single molecules (“monomers”); above it, vesicles are formed. The vesicles remain in equilibrium with monomers at a concentration equal to the CVC. Note that amphiphile systems can exhibit more complex equilibria. (Inset) Epifluorescence micrograph of vesicle structures visualized with Nile red, a hydrophobic dye. These systems are used in the laboratory to model protocell compartments. Scale bar = 20 µm. (B) Hydrophobic or hydrophobically derivatized photosensitizers inserted in the protocell compartment boundaries: (1) amphiphilic ruthenium tris-bipyridine; (3) amphiphilic [Fe–Fe] cluster; (5) perylene; (6) 2,3(a)-naphthopyrene. Both (5) and (6) are polycyclic aromatic hydrocarbons (PAHs). (C) Hydrophilic solutes or nanoparticles in the aqueous lumen of protocells: (2) ruthenium tris-bipyridine; (4) [Fe–Fe] cluster; (7) (upper) inorganic pyrophosphite, (lower) inorganic pyrophosphate; (8) mineral particles. (D) An electron transfer system across decanoic acid vesicle bilayers. PAHs, such as (5) and (6), in the compartment boundaries can be excited by light and deliver an electron to an acceptor (here ferrocyanide). The PAH radical cation can be regenerated via electron transfer from a sacrificial electron donor, like ethylenediaminetetraacetic acid (EDTA), in the external medium. This results in net transmembrane electron transfer (Cape et al. 2011).

Internal Catalytic Network and Information System

A protocell should be able to harbour within its compartment reactions that produce its own building blocks. From its simplest form, based on encapsulated metal-ions and complexes or even mineral particles, this reaction system would have gradually evolved first into RNA-based and, over time, into protein catalytic networks, i.e. towards metabolic bio-machinery.
Small organic molecules of various compositions can be produced on mineral surfaces (Cody 2004). The minerals in question participate in the synthesis, either by being a supporting matrix (through specific adsorption), or as a reactant (e.g. redox reactions involving FeS), or as a true catalyst (in the Fischer–Tropsch type syntheses). Thus, mineral particles once encapsulated into a protocell compartment could have carried out these syntheses. The current presence of iron sulfide clusters in enzymes clearly supports such a concept (Mansy et al. 2016 this issue).

Mineral surfaces, such as those of clays, could also have promoted the emergence of biopolymers. Biopoly­merizations are condensation reactions that are not favoured in an aqueous environment, even at extremely high monomer concentrations. Amino acid and activated nucleotide monomers could have first adsorbed on mineral surfaces, either spontaneously or as the result of a drying process. Both types of monomers could then be successfully, and non-enzymatically, polymerized (Hill et al 1998; Maurel and Leclerc 2016 this issue). Recently, an indirect support of chemical reactions by mineral surfaces was also demonstrated by Rajamani et al. (2008): in this case, the dehydration/rehydration cycles of nucleotides in the presence of lipids on solid surfaces led to significant polymerization at relatively mild temperatures; the rehydration of the “dried” films even permitted a partial encapsulation of the biopolymeric products.

Thus, mineral surfaces could have jump-started the emergence of the main constituents of the current biochemistry, provided that some form of selective adsorption was possible. Selective adsorption of chiral molecules on chiral mineral surfaces has been demonstrated by Hazen et al. (2010).

Energy Harvesting

The uptake of energy and its conversion into bioenergetic currency (as in the respiration) or chemicals (as in photosynthesis) is central to cellular metabolism. However, a significant problem in the field of abiogenesis concerns the emergence of a phosphorus-based bioenergetic system or the development of the chemical machinery needed for photosynthesis from primitive chemical machines within putative early Earth environments and without any sophisticated (proteinaceous) catalysis (Serrano et al. 2004).

Heat would have been the simplest energy to convert into chemical energy for early protocell systems, but it comes at a cost. Heat tends to destabilize amphiphile structures (Walde and Monnard 2015). In the case of light energy, simpler systems that are light-active could have functioned as primitive pigments, e.g. polycyclic aromatic hydrocarbons (PAHs; see Fig. 3) (Cape et al. 2011) whose presence in chondrites and within interstellar environments has been confirmed. These molecules spontaneously insert into vesicle bilayers. Other metal complexes, such as ruthenium and related complexes (Walde and Monnard 2015), if present, could be building up reaction units. Moreover, photosensitive minerals, such as the geologically available titanium dioxide (Summer and Rodoni 2015), could also serve as light-conversion units. In the case of redox-active minerals, iron sulphides would have been available. Thus, in principle, primitive energy harvesting units to power the direct transformation of chemical precursors into protocell units are plausible. These photocatalysts would be able to produce amphiphiles or even the ligation between nucleic acid strands (Walde and Monnard 2015), as well as power the formation of energy currency (Summer and Rodoni 2015). Moreover, PAHs do induce vesicle division (i.e. the splitting of a protocell into two protocells), which is an essential step in self-replication (Zhu et al. 2012).

It is important to remember that the chemical inventory was much more complex than the chemical composition of current cells. For instance, the total number of amino acids in meteorites is around 80; but life is based on a mere 20. By contrast, it is also clear that the presence of additional chemicals may have contributed to the emergence of protocells. As an example, the addition of co-surfactants, such as fatty alcohols or even PAHs, to fatty acid structures extends structure robustness in terms of aggregation equilibria, pH, temperature sensitivity, and solute encapsulation (Walde and Monnard 2015). Primitive mixed compartments might have even had an evolutionary advantage compared to pure ones (Budin and Szostak 2012).

PROTOCELL CONSTRUCTION

The involvement of mineral surfaces would have been crucial in providing a nurturing environment for protocell formation. The formation of protocells, as is still the case for the current cellular membranes and other protein assemblies, would have been driven by molecular self-assembly processes, which are dependent on environmental conditions (pH, ionic strength, temperature) and, most importantly, on the properties of the molecules themselves and their concentrations (Sahai et al. 2016 this issue; Schoonen and Smirnov 2016 this issue).

Self-Assembly Processes and Protocell Stability

Besides being potential compartments themselves, minerals could have supported the formation of other types of compartments, such as amphiphile vesicles. Many mineral surfaces promote vesiculation (Hanczyc et al. 2007): in this case, a mineral’s surface facilitates bilayer formation by likely promoting ordering of molecules on their surfaces in specific configurations.

The co-localization of protocell subsystems into protocell compartments might have been induced by mineral surfaces. Indeed, clay particles can both promote the synthesis of RNAs (Maurel and Leclerc 2016 this issue) and the vesiculation of amphiphiles (Hanczyc et al. 2007), even when RNA is associated with a clay’s surface. That is, polymers whose uptake by passive diffusion across amphiphile bilayers is limited could have been produced in situ, only requiring the diffusion of monomers, which is usually large. The same idea should apply to short peptides and other molecules of interest.

Titanium oxide particles promote the formation of amphiphile bilayers on their surfaces, a process that has been proposed as a way of linking mineral chemistry to protocell systems, which in turn links a potential source of chemicals and energy with cell-like boundaries (Summers and Rodoni 2015).

PROTOCELL EVOLUTION

It is clear that minerals and geochemistry played a paramount role in the emergence of early protocells. The question remains, however, about the processes that led to how protocells escaped from a mineral’s surface and became suspended as an autonomous system in an aqueous medium. Even though it has been suggested that cellular systems can completely mature in the presence of FeS (Martin and Russell 2003), several essential issues make these processes unavoidable: 1) Direct interactions between polymers and surfaces increase as the length of the polymers increase, resulting into an ever-tighter association which could have prevented the polymers from folding and becoming active catalysts; 2) Not all cellular functions, including protocellular ones, can be carried out on a mineral’s surface, especially considering the intertwined nature of cellular pathways; 3) Environmental changes would have required “migration” of protocells towards more auspicious environments; 4) One mineral would not have produced all the potential catalytic sites necessary for protocell construction and function, never mind subsequent evolution. Although the mineral heterogeneity and large inventory might have afforded a larger network of potential catalytic sites, developing a complete protocell system purely using mineral substrates seems most unlikely.

Prerequisites for Evolution

To evolve from their simple embodiments towards full-fledged precellular systems, protocells must have the ability to preserve their composition and functions, transmit them to next generations, and acquire novel functions by either taking up novel molecules from the environment or by merging with other protocells. It seems very unlikely that the transmission of protocellular properties to a new generation was directly linked to the heritable information system that encodes to the system’s chemical composition, as in the genetic system now ubiquitous in modern biology. It is more likely that the first compositional information, and most importantly the functions that derived from it, defined how the whole protocell system could be replicated, which is possible even with simple protocell systems (Albertsen et al. 2014). Darwinian evolution could then have been driven by the maturation of the RNA system (Szostak 2012).

Compartmentalization

The evolution of the compartment subsystem was driven by the availability of amphiphiles, that either alone or in association with other molecules (such as PAHs) would have formed more stable vesicular compartments. The emergence of amphiphiles that possessed longer hydrocarbon chains or double hydrocarbon chains would have ensured better compartment integrity and protection for its contents. However, this would come at a price: the reduction of the protocell’s ability to take up molecules from the environment. Nevertheless, a simultaneous advantage of a stronger compartment boundary is that there would be a permeability decrease that would enable chemical gradients across wall boundaries to emerge, thereby initiating some novel energetics that could be exploited.

Internal Catalytic Network and Information System

In every phase of their evolution, protocells would have been dependent on environmental chemical fluxes (chemical syntheses, temperature, dehydration/rehydration cycles). However, protocells must have developed reaction networks that covered their chemical needs. To determine whether an RNA-based catalytic network and information system could have co-emerged, the problem needs to be addressed in relation to the compartmentalization of RNA in amphiphile vesicles. The encapsulation of RNA strands during their production on minerals, or even after their production, could have occurred on the early Earth during cycles of dehydration/rehydration (Ramani et al. 2008).

Once encapsulated into a vesicle, the expansion of functions would have been difficult without either transient vesicle disruption or merging of vesicles, even though non-enzymatic, template-directed polymerization of RNA (copying an RNA fragment) is possible within a vesicle (Walde and Monnard 2015). Indeed, more complex catalytic activities require longer ribozymes (RNA catalyst) whose copying in bulk aqueous solution or on a mineral surface has yet to be demonstrated. Maybe ribozymes were assembled from smaller RNA fragments (Doudna et al. 2001), which would have been more readily available. Ribozyme assembly, function and replication would have been promoted by other smaller molecules and metal ions, all of which require a suitable medium for the necessary reactions. Thus, the development of robust RNA metabolism seems to require the presence of an aqueous environment.

Energy Uptake

Protocells breaking off from their mineral substrates may have been the trigger for the development of more complex energy harvesting units and the advent of activated phosphorus-based energy-currency molecules, which are the drivers of much of the metabolic activity of contemporary biochemistry (Serrano et al 2004). The formation of energy currency molecules would have been necessary for the development of a robust “metabolism” because of the need to precisely time chemical production, which the protocell would need to survive. Thus, the emergence of phosphorus-based bioenergetics should not be considered solely as a geochemical outcome but as a consequence of environmental conditions and contingent, system-specific properties of protocell compartmentalization.

The phosphorus bioenergetics can be understood in terms of four interlinked processes: (i) harvesting external energy (light, minerals, etc.); (ii) generating an electron gradient; (iii) pumping of protons across a semi-permeable membrane (driven by the electron gradient); and (iv) capturing of free energy (free energy associated with the charge and concentration gradient dissipated upon return passage of protons through the transmembrane protein complex) within the molecular disequilibrium between inorganic phosphate (Pi) and condensed inorganic phosphates [pyrophosphate (PPi)], or nucleoside triphosphates [e.g. adenosine triphosphate (ATP)]. Interestingly, these bioenergetic processes require compartmentalization to co-locate chemical systems (e.g. the light harvesting molecular apparatus) and confine the products. The compartmentalization prevents the dissipation of gradients.

For protocells devoid of sophisticated trans-bilayer transport systems, such permeability would have been essential to ensure access to molecules produced abiotically in the environment. Thus, the properties of these compartmentalization systems seem, at first sight, to preclude the formation of molecular gradients. However, comparisons between various solute diffusion rates show that there is a low permeability of charged small polymers (such as nucleic acids), of small anionic solutes with high charge density (such as potassium ferricyanide) (Cape et al 2011), and of pyranine (a fluorescent dye). Thus, molecular gradients of these molecules, or comparable ones, can be retained for periods of time compatible with further use of their stored energy for other chemical reactions (Fig. 3).

Conclusions and outlooks

The involvement of geology and geochemistry in the emergence of life is undisputable, as is that of chemical systems. Each field has contributed greatly in advancing our knowledge of how life might have arisen. But protocell research still lacks an overall strategy by which to solve the cornerstone questions about how protocells originated. To move forward in this field, more collaborations between the researchers are needed.

As our understanding of prebiotic chemistry and geology broadens, it becomes clear that a resolution of the question of how protocells arose will not come from a single field, but rather from a concerted effort at the interface between many fields. The main challenge is the chemical complexity of the system and finding the appropriate research methodology. Current investigations, for example, are trying to implement cellular functions into a geochemical context. This approach is logical because the product of protocell evolution is known—it is the cell. However, the current assumption that protocell to cell evolution is a relatively linear process might yet turn out not to be correct.

Acknowledgments

The authors thank colleagues in Odense (Denmark) and in Leeds (UK) for fruitful discussions, as well as the members of the COST [European Cooperation in Science and Technology] Action TD 1308 program, “Origins and Evolution of Life on Earth and in the Universe”.

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