Living entities exhibit the three fundamental characteristics of metabolism, growth and reproduction, to which we may add evolutionary adaptation to their environment. Understanding how life having these characteristics emerged on Earth within 1 Gyr of its formation is both a fascinating scientific problem and a pre-requisite for predicting the presence of life elsewhere in the Universe. At the Discussion meeting on the conditions for the emergence of life on the early Earth, held at the Royal Society, 13 and 14 February 2006, scientists from several disciplines discussed the origin of the biotic raw materials, and the conditions and dynamic processes involved in the genesis and the early evolution of primitive life forms. This issue of Philosophical Transactions B contains the papers presented at the meeting, short accounts of which are given in this Introduction. Questions to the speakers, and their responses, are presented immediately following each paper. In reflecting on the issues discussed, it is well to remember that extremely long periods of time, of the order of millions and of billions (giga) of years are involved, periods which are conceptually difficult to envisage in terms of our everyday cognizance of dynamic action and change.
The first session was mainly devoted to the study of molecules in prebiotic settings, beginning with the paper by Thaddeus (2006) on prebiotic molecules observed in the interstellar gas by astrophysical spectroscopy, principally in the radiofrequency region. After rapidly detailing the known interstellar and circumstellar molecules, with emphasis on those containing the most abundant biogenic elements, Thaddeus mentions the positive qualitative and quantitative analytical capacity of radioastronomy for identifying interstellar species and determining their physical environment. The problems discussed concern the possible identification of interstellar aminoacids, as well as of polycyclic aromatic hydrocarbons (PAHs) which have been suggested to be the most abundant organic molecules in the Universe and which may be stepping stones to building up interstellar grains. However, the negative result of an astronomical spectral search for the known microwave spectrum of corannulene puts the PAH hypothesis in jeopardy until specific PAHs are identified by astronomical spectroscopy.
Bernstein (2006) reviews the possible terrestrial formation mechanisms of pre-biotic organic molecules, such as by Miller–Urey synthesis, and in hydrothermal vents, which he somewhat favours. He also considers the input of prebiotic material from space in the form of meteorites, micro-meteorites and interplanetary dust particles originating in comets and asteroids. The types and abundances of organic species that were formed on or off the Earth are discussed, in particular, in the context of possible processes leading to the formation of amino acids, sugars, amphiphiles, etc., which could be directly related to the origin or the early evolution of life. In a more speculative mood, Bernstein considers briefly the problem of distinguishing between abiotic organic molecules from those that are actual signs of life, as a part of a robotic search for life in the Solar System.
Grady & Wright (2006) discuss carbon cycles on the early Earth, and more speculatively, on Mars, in terms of a complex interaction between the atmosphere, the hydrosphere and the lithosphere, and eventually with a reactive biosphere. The factors maintaining in balance the Earth's carbon inventory are currently absent in Mars, but may have existed in the past. The Earth's carbon cycles have changed as its tectonic structure and its biological content have evolved. Knowledge of this evolution, adapted to a Martian context, and consideration of the sources and sinks of carbon on Mars based on the carbon chemistry of Martian meteorites, make it possible to investigate evidence for a Martian biosphere. At the present time there appears to be little such evidence.
If life exists or existed on Mars, what are its possible signatures? This subject is presented by Anand et al. (2006). For life to survive, the presence of liquid water is thought to be essential. Recent space missions have reinforced earlier suggestions that Mars was once warmer and wetter, and have also suggested that the Martian landscape was shaped by processes similar to those operating on our own Earth. Evidence of past aqueous activity on Mars can be obtained through mineral, chemical and isotopic studies of primary and secondary minerals in Martian meteorites. This paper includes studies of the action and effects of water on Mars by using as diagnostic the fractionation of iron isotopes, which can be significant during low-temperature alteration processes. The biological influence on fractionation is currently under investigation. The results might be used to distinguish, for example, low-temperature abiotic processes from biological activity on Mars.
The physical and chemical conditions on the early Earth were subjects of the second session, which opens with a contribution by Lunine (2006) who begins by tracing the various events and factors that led to the formation of the Earth, including collisions with large bodies. There occurred a complex early history of infrequent, catastrophic, giant collisions against a background rain of impacts from more numerous and smaller debris in the Hadean period (4.56–4.0 Gyr ago) during which the Moon was born in the very early stages via a collisional process. Computer simulation of the processes leading to the formation of the Earth and the Moon has advanced our knowledge in this area. Lunine discusses various sources of water on the Earth and considers how, as accretion tailed off and the Earth's crust cooled, surface liquid water became stable within 500 Myr of Earth's origin, perhaps sooner. The presence of water and high heat flows, coupled with other conditions different from those of today, has significant implications for the atmosphere and for the chemistry of organics, including those at the oceanic geothermal sites. The possibilities and interest of exploration of Venus, Io, Europa and Titan as planetary analogues of the early Earth environment are presented.
The atmospheric composition and climate on the early Earth are important factors determining the emergence of life and the nature of primitive organisms. Kasting & Howard (2006) discuss the early atmosphere and climate, the data being based mainly on analyses of oxygen and sulphur isotopes in various materials from the Archaean and Proterozoic epochs, and also on evidence for global glaciation periods in the Proterozoic. They argue in favour of a temperate early Earth, possibly during the period when life arose, rather than the previous estimates of 45–85°C for surface temperatures. An important factor in the argument for a temperate early Earth concerns changes in seawater isotopic composition, a new mechanism for which is outlined. Warm, temperate and ‘snowball Earth’ conditions are considered as having existed at various epochs, reasons for the changes of climate between hot and cold being the matter of study and speculation. These changes have implications for the development of life as well as possibly reflecting the effects of life on the climate.
With the contribution of Schwartz (2006), we enter detailed discussion of the synthesis of compounds that have fundamental biochemical functions. He stresses the importance of prebiotic synthesis of phosphorus-containing species such as nucleotides and polynucleotides for the emergence of life. This synthesis requires not only a geological source of reactive phosphorus compounds, but also reasonable pathways for their incorporation into chemical systems on the primitive Earth. Schwartz shows that for the mineral apatite, which is the principal source of phosphate on Earth, there are at least two pathways that overcome problems of low solubility and reactivity. The mineral schreibersite in meteorites is a possible extraterrestrial source of reactive phosphorus.
Possible steps leading from abiotic chemistry to a living entity were the subject of the third session, which dealt with the development of biology. It began with a paper by Taylor (2006) on conceptual and molecular model studies bearing on the origin of transcription and translation of information in an RNA world, a biological world prior to protein synthesis whose conceptual possibility was much enhanced by the discovery that RNA molecules can possess catalytic activity. His approach avoids difficulties or certain inefficiencies in the RNA-copying process and in particular the necessity of mechanisms for keeping separate the template RNA strand and its reverse complementary transcript in order for the parent self-replicating RNA to discriminate its own sequence from all others. Taylor's solution involves synthesis of a parallel complementary copy of the RNA polymerase. The results of model simulations suggest that an operational temperature up to 90°C would allow a replicase using a parallel complement to be viable. This molecular model leads to proposals for the structural nature of the replicase. The function of a replicase requires it to bind both a template and a transcript along with a nucleotide monomer, difficult to achieve with known ribozyme structures. Taylor proposes that this requires a ribosome as a suitable structure containing the required active sites. The final model incorporates the synthesis of a polypeptide chain regulated by tRNA-like molecules that impose a ratchet mechanism in steps of three bases along a template.
The contribution of Szathmáry (2006) also deals with the origin of informational replicators (of which genes are but an example) and reproducers, which are necessary for biological evolution to occur. The appropriate selection dynamics and chemical conditions are considered. The importance of the error threshold in copying fidelity is emphasized. A non-informational replicator, such as an intermediate in the formose reaction, is used as a model to discuss the decay threshold. After a discussion of infrabiological systems, which are systems lacking one of the key subsystems of life, such as a metabolic subsystem, and defining composomes (a group of molecules each exerting some catalytic function within a lipid context), Szathmáry uses these concepts to create dynamic models of (pre)biotic growth and evolution. He then develops a model based on chemical reactions occurring on a chromatographic column considered as a series of connected cells. This chromatographized replicator model, which could be subject to experimental test, is considered by Szathmáry to be relevant to the origin of life on Earth. The coexistence of unlinked replicators constituting a primordial genome is shown to be possible by involving various factors, including chaotic flows, surface dynamics and compartmentalization.
The next few papers, although harnessed on theoretical concepts concerning the formation of basic biochemical components in the emergence of life, are firmly based on experimental studies of the relevant physicochemical processes. After a brief discussion of possible sources of the reduced compounds on the primitive Earth, Ferris (2006) describes the clay-catalysed formation of RNA oligomers. Montmorillonite which, on Earth, can be formed by the weathering of volcanic ash, and which has recently been detected on Mars, is capable of catalysing the formation of oligomers of RNA that contain up to 50 monomer units. It is also capable of catalysing vesicle formation. The processes studied exhibit sequence selectivity, which restricts the number of oligomer isomers formed, regioselectivity in phosphodiester bond formation and homochiral selectivity in dimer formation. The preferred possible role of selective catalysis, as compared with specific catalysis on a specific substrate, is discussed in terms of its bearing on the origin of life.
Wächtershäuser (2006) develops his theory of a chemi-autotrophic origin of life in a volcanic iron–sulphur world. This postulates a pioneer organism of life, which emerged at sites of reducing magmatic exhalations approximately 4.4 billion years ago. The first living organism, the so-called pioneer organism, a starting point in evolution, is characterized by an inorganic substructure that is catalytically active. It promotes the growth of an organic superstructure lying within a volcanic liquid water phase that is the source of chemical nutrients. The pioneer organism is shown to have potential for growth, for reproduction by ligand feedback and for evolution by double catalytic feedback. The experimental studies of various chemical stages are described. The development of cellularization via lipid synthesis and bilayer membrane formation is discussed, along with polycondensation, enzymatization and nucleic acid replication. The chemi-autotrophic model, involving a direct mechanism of evolution by variation of peptide synthesis and peptide feedback, developed later into an indirect, stochastic, genetic mechanism involving variations of mRNA sequences due to replication variations. A discussion on the pre-cell concept of Kandler leads to the conclusion that all forms of life from the pioneer organism to the pre-cells must have been hyperthermophiles. The possible evolution of pre-cells into the bacteria, archaea and eukarya domains is described. The evolution of life, usually thought of in terms of adaptation to its environment, is characterized by an increase in molecular complexity, which has its origins in the nature of redox chemistry active in the metabolic processes prevalent in the pioneer organism.
Modelling self-assembly processes in the prebiotic environment is the theme of the contribution of Deamer et al. (2006). They discuss related themes that can be used to guide research on the origin of life. The first concerns its site on the early Earth, where liquid water, appropriate organic compounds, and an adequate source of the energy required to carry out synthetic reactions must be available. The second theme concerns chemical and physical properties of the organic compounds available to participate in the origin of life, in particular, their capacity for polymerization and their amphiphilic quality, a property that permits self-assembly into membrane-bounded compartments that can encapsulate molecular components, thus forming microscopic reactors. Deamer et al. report recent studies in which self-assembly processes of organic compounds were investigated in two natural geothermal environments (Kamchatka and Mount Lassen), where the hot spring sites include boiling clay-lined ponds. These ponds are possible manifest variants of Darwin's offhand suggestion of a ‘warm little pond’ for the site of the first production of a living organism. The experiments followed the physicochemical fates of a set of suitable organic solutes and phosphate, forming a possible prebiotic mixture, which were added to these acidic ponds. The results showed that the organic compounds were adsorbed onto clay surfaces, impeding chemical reactions between them, and that self-assembly of boundary structures cannot occur under hot acidic conditions. It was concluded that the most plausible environment for the origin of life would be an aqueous phase at temperatures not above 60°C and of low ionic strength. These characteristics are very different from those of other proposed sites for the origin of life, such as geothermal or marine environments.
In the final session, devoted to early ecosystems and manifestations of early life, the paper by Canfield et al. (2006) discusses anoxic ecosystems in the early Earth. These include ecosystems involving the cycling of hydrogen and methane as well as a variety of iron, sulphur and nitrogen compounds. From the structure of these systems and the source strength of electron donors and acceptors, whose availability for fuelling early anaerobic metabolisms is explored, it is possible to estimate that the primary production rates of the ecosystems in the ancient biosphere would have been much smaller than in today's biosphere. Oxygenic photosynthesis, which originated with the evolution of cyanobacteria, is the dominant factor in biological activity today. Its arrival some 2 Gyr ago dramatically modified the diversity and the magnitude of life on the Earth. The geological record, examined as to its clues concerning the activity level of the ancient biosphere, including the carbon cycle, favours an Fe-based anoxygenic photosynthetic ecosystem in the early Archaean. A carbon cycle driven by oxygen photosynthesis, where the oxygen produced is removed by reaction with reduced species in the Earth's mantle, thus maintaining an anoxic atmosphere, is also thought to be possible.
Stetter (2006) reviews the role of hyperthermophiles in the history of life. Hyperthermophilic bacteria and archaea have been observed within terrestrial, subterranean and submarine high-temperature environments occurring mainly along tectonic spreading and subduction zones. They exist essentially in anaerobic environments, where they gain energy by inorganic redox reactions involved in a chemolithoautotrophic mode of nutrition. Stetter discusses examples of recently discovered hyperthermophilic archaea, in particular, a group of small ‘nano-archaea’ which might have existed on the early Earth. The position of hyperthermophiles within the phylogenetic tree of life provides evidence for the last common ancestor (LCA) to have been a hyperthermophile. Furthermore, they are known to survive deep-freezing at −140°C, so that within impact ejecta, they could have at least survived the temperatures associated with transfer to other planets and moons through cold space.
The consequences of the considerable impact bombardment of the early Earth on the origin and the emergence of life are discussed in the contribution of Cockell (2006). The craters formed by asteroid and comet impacts are possible favourable sites for prebiotic chemistry during the Hadean epoch, possibly mimicking a version of Darwin's ‘warm little pond’. In these sites can occur the formation of various metal sulphides, clays and zeolites which can act as templates for prebiotic reactions. Non-acidic hydrothermal conditions can favour molecular binding to mineral surfaces, while intense fracturing of rock during impact can create extensive surfaces for chemical reactions to occur. Meteorite impact deliveries can provide further substrates for prebiotic reactions, and the existence of diverse impact energies from incoming objects could result in different rates of hydrothermal cooling. Furthermore, the variety of impacts could lead to many different sets of local environment conditions and so provide the circumstances for what is virtually a large number of different ‘experiments’ concerning the origin of life. The physicochemical conditions in a range of crater sites are explored in the context of prebiotic reactions that lead eventually to early life. Cockell presents a possible overall scheme for the origin of life within impact craters, all the way from prebiotic reactions to the emergence of self-replicating systems, remarking that similar prebiotic processes could be sought in Martian impact craters. The craters are shown to provide habitats protected from environmental extremes, which can support the growth of diverse organisms, relevant in particular to the existence and growth of microbial communities on the early Earth.
Before the presence of oxygen, generatix of protective ozone, in the atmosphere, the Earth was bathed in UV light, which should have been destructive of life forms. Westall et al. (2006) investigate the UV conditions on the early Earth as indicated by the existence and formation of 3.4 Gyr old filamentous microbial mats, and rod and vibroid structures embedded in a smooth film, found as fossilized structures in shallow water sediments in South Africa and considered to be formed by anoxygenic photosynthetic micro-organisms. The biogenic nature of the fossils is demonstrated by methods that clarify the necessary geological, physical and chemical tests for differentiating them from abiogenic artefacts or more recent contaminants. The structure of the microbial mats is analysed to provide information on the fossilization process and the state of the organic matter within it. The morphological, chemical and other characteristics of the mat components are the same as those of modern micro-organisms, including colony and biofilm formation. Interaction of the biofilms with the local environment of sediment particles and flowing water, as well as desiccation and rapid silification processes are shown to have occurred. The filamentous microbial mat and the rod/vibroid colony appear to have been in a healthy state when fossilized, although they were directly exposed to the atmosphere. A thin organic smog formed by photolysis of methane could have helped to provide UV protection of the early micro-organisms.
The conclusion to a very lively meeting is given in a paper by Jortner (2006), who summarizes the nature of the presentations, and embeds some of them in discussions on the origin of prebiotic chemicals and on the conditions and constraints for life to appear. He also presents his reflections on models and processes concerning the emergence of life. He emphasizes structure–function relationships in biology, complemented by dynamic energy transfer aspects. The development of increasing complexity of matter from the elementary chemical bricks up to functional living entities is sketched. The essential knowledge gap in this holistic framework is the passage from self-organized complex matter to living matter. Bridging this gap requires that we reach an adequate definition of life, a task explored but shown to be difficult to achieve with entire satisfaction. The concept of molecular information is discussed and its role in information-driven self-organization (self-assembly) processes of matter, eventually allowing for selection, evolutionary adaptation and self-reproduction, is explored in terms of the relevant physical chemistry. The subject of impact events is discussed in some detail and new pertinent information on laboratory experiments involving the impact of high-energy clusters on solid surfaces is described and its possible relevance to astronomical impact events is evoked. The simulations involving the extreme physical conditions in such laboratory experiments could be of interest for producing the building blocks of biomolecules.
Jortner sketches two different approaches to considerations on the origin of life. The bottom-up approach involves the nanofabrication of biomolecules by catalysis of their chemical building blocks, whose nature depends in part on the atmospheric conditions and energy sources on the early Earth, followed by self-organization leading eventually to complex biological matter. The problem of encapsulation of biochemical components of biotic significance, eventually in cell structures, is discussed. An analysis is made of the need and the methods for restriction of compositional and conformational redundancy in the synthesis of proteins and nucleic acids. The top-down approach also emphasizes the role of self-organization, but approaches this question in the reverse order, i.e. by deconstructing functional living matter to small units that still exhibit biological functions, and also by determining phylogenetic relationships down to the LCA and beyond to the minimum set of genes necessary for cellular functionality. In a concluding section, Jortner evokes several open questions in the origin of life story, among which are: (i) the origin of biomolecular chirality, (ii) the need for much more experimental testing of theoretical models of self-organization processes, (iii) understanding the prebiotic origin of RNA, (iv) clarifying the properties of the LCA, (v) determining the level of molecular–supramolecular–nanostructural complexity required for biological function to become manifest and (vi) clarifying the time-scales for the emergence of life in the context of cosmological and geological dynamic factors.
One contribution of 19 to a Discussion Meeting Issue ‘Conditions for the emergence of life on the early Earth’.
- © 2006 The Royal Society