Energy Sources, Self-organization, and the Origin of Life
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The emergence and early developments of life are considered from the point of view that contingent events that inevitably marked evolution were accompanied by deterministic driving forces governing the selection between different alternatives. Accordingly, potential energy sources are considered for their propensity to induce self-organization within the scope of the chemical approach to the origin of life. Requirements in terms of quality of energy locate thermal or photochemical activation in the atmosphere as highly likely processes for the formation of activated low-molecular weight organic compounds prone to induce biomolecular self-organization through their ability to deliver quanta of energy matching the needs of early biochemical pathways or the reproduction of self-replicating entities. These lines of reasoning suggest the existence of a direct connection between the free energy content of intermediates of early pathways and the quanta of energy delivered by available sources of energy.
KeywordsBiological minimum energy quantum Coupled reactions Energy barriers Free energy Photolysis Self-organization Thermolysis
Since attempts to make life initiate from scratch are likely to remain beyond the reach of science in the near future, the origin of life is one of the most stimulating questions among those in relation to the emergence of self-organization (von Kiedrowski 2001). The mere possibility of achieving this target is dependent on the reliability of the alternative between two opposite philosophical positions about the role of contingency in the process. The first one has been supported by Christian de Duve (1996) who claimed that Life is a cosmic imperative, whereas Jacques Monod (1970) considered that it is the result of a succession of highly improbable events. The latter position leaves almost no room for scientific investigation since it is meaningless to build laws from a single successful event resulting from chance only or to perform experiments with almost no possibility of success. The former one encompasses the idea that driving forces are capable of inducing simple physicochemical processes to generate self-organized sub-systems of increasing complexity.
But, it is more likely that contingency played a major role together with driving forces in inducing self-organization, which is consistent with its essential role in creating the diversity responsible—with selection—for biological evolution. Moreover, a contribution of chance is mandatory in any historical process, so that a scientific description of self-organization must involve a combination of driving forces and non-deterministic events. Self-organization in chemical systems is rooted in the discontinuity of matter at the atomic/molecular scale, but two main strategies to get macroscopic heterogeneity in molecular assemblies are available. The first one is to allow molecular building blocks to interact in a non-covalent way to give crystals or supramolecular structures (micelles, aggregates, and more or less precisely defined supramolecular architectures). These structures are usually under thermodynamic control since the formation of non-covalent interactions commonly involves low kinetic barriers—except when a strong interaction is the result of the cooperation of multiple weak interactions leading to entropically stabilized structures (Jencks 1981; Hunter 2009). The second one results from amplification processes, and it is revealed by the observation of molecular assemblies adopting collective dynamic behaviors, as for instance chemical waves (Biosa et al. 2006), which are reminiscent of the organization of metabolic complexity, rather than simply formed by static, ordered spatial arrangements. The development of experimental and theoretical investigations now allows the proposal of increasingly detailed scenarios for the emergence of biological organization. If we consider the description of life as corresponding to a state of matter driven by the dynamic stability of self-reproducing chemical systems (Eigen 1971; Eigen and Schuster 1977; Eigen et al. 1988; Pross 2005; 2009; Wagner and Ashkenasy 2009), then any energy exchange must take place at the molecular level. In chemical systems leading to the emergence of life, energy is likely to have been brought about by energy-rich molecules (chemical energy) and released in the environment as heat or inactivated waste materials. The following question that we intend to address here is to determine whether these requirements have some consequence for the nature of the chemical systems involved. This report is devoted to identify the main properties conferring to energy sources or organic energy carriers the essential features supporting the emergence of self-organizing systems based on organic molecules. Taking into account, on the one hand, the fact that exchanges of energy take place through finite quanta and irreversibility leading them to be dispersed into less concentrated forms and, on the other hand, the biological free energy requirements of purported early pathways, we recognize processes starting from thermal or photochemical lyses of gaseous species in the atmosphere as presenting the attributes needed to induce biomolecular self-organization.
Self-organization and the Second Law
The spontaneous formation of order from disorder is in contradiction with the common sense, which is expressed in thermodynamic language by the Second Law stating that entropy tends to increase in an isolated system. Then, chemical systems spontaneously evolve toward the equilibrium state in which the concentrations of chemical species are determined by their relative energy levels and statistical rules. To remain in a non-equilibrium state, a self-organizing system must be open or at least closed (exchanging matter and energy, or energy only with its environment, respectively) (Kondepudi and Prigogine 1998), in which case, the entropy loss associated with the formation of a structure is compensated by the increase in disorder in the environment in such a way that the overall entropy increases (Schrödinger 1946; Plasson and Brandenburg 2010). It follows that exchanges of energy and/or matter are needed as a starting point for self-organization dynamics. In a locally closed system (exchanging only energy with its environment) at the steady state, the amount of energy (measured as enthalpy ∆H) that enters the system must be identical to the amount that is released, but possibly with a strong increase in entropy, i.e. requiring that energy is released under a more “diluted” form than when entering the system (this is the case for instance of the Earth, the surface temperature of which is regulated so that the solar energy received as light is compensated by radiation at longer wavelengths). This can be expressed in different terms by considering that self-organization in a closed system requires the conversion of "low entropy energy" into "high entropy energy" (usually heat).
A Minimum Quantum of Energy in Biology
Standard free energy of hydrolysis of common biochemical intermediates / functional groups at pH 7 and 25°C
∆G°' / kJ mol−1a
Acetyl coenzyme A (thioester)
ATP (to ADP & Pi)
ATP (to AMP & PPi)
Aminoacyl-tRNA (amino acid ester)
Glycine ethyl ester
Amino acid thioester
Chemical Energy Sources
Thermal Energy and Photochemistry
Standard free energy of reaction (hydrolysis unless otherwise mentioned) of potential prebiotic energy-rich low-molecular weight compounds at pH 7 and 25°C
∆G°' / kJ mol−1 a
HC ≡ CH (g)
Alanine nitrile (aq)
Alanine (aq) + NH3 (aq)
HC ≡ N (aq)
N = C = O−
HCO3−+ NH3 (aq)
HCO3−+ NH4+ + NH3 (aq)
S = C = O (g)
CO2 (aq) + H2S (aq)
FeS (s) + H2S (aq)
FeS2 (s) + H2 (g)
This discussion was intended to demonstrate that it is possible to get new insights by encompassing both the representation of life as a state of matter governed by the dynamic stability of self-reproducing systems (autocatalytic loops, replicators) and the free energy requirements of early biochemical processes. It allows building scenarios of life's emergence in which every step is under the control of a driving force acting in selecting, among the variety of reproducing components arising as a result of independent (contingent) events, those whose population increases faster in an environment constrained by the availability of matter and energy sources. Considering that present day biochemistry conserve some of the essential intermediates that were present in early living organisms allows to identify the upper range in which early biochemical energy transfer were working at those times. We have proposed here that only a certain kind of chemistry could feed these biochemical processes through coupled reactions and metabolic cycles. This proposal, consistent with the idea that early organisms were unable to concentrate energy at the molecular level (operating a kind of thermodynamic engine) but depended on spontaneous energy flows, results in a correspondence of the free energy quanta exchanged in biochemical pathways with the requirements in terms of the quality of the supply in energy. However, these views present a limitation because usual metabolic cycles do not present the variability needed for a non-limited accumulation and storage of information, which has given support to criticism (Orgel 2008). In contrast, this limitation would not have been present with systems that involve genetic polymers capable of accumulating information in their sequence though their replication obeys specific features (von Kiedrowski 1986; Szathmáry and Gladkih 1989; Szathmáry and Maynard Smith 1997; Szathmáry 2000). Anyway, and independently of the debate upon whether metabolic or genetic features were essential for life emergence, in the case of genetic replicators, energy is also needed to form activated monomers from simpler precursors. The possibility that activated ribonucleotides may have been formed through stepwise downhill processes from low-molecular weight precursors has received some grounds (Powner et al. 2009). But, the process may be greatly improved by the assistance of a larger metabolic network having a wider scope of chemical abilities and cooperating with genetic polymers to increase the availability of energy for the replicating system in a way consistent with the ideas developed by Gánti (2003). Experimental indications that peptide precursors such as α-amino acid N-carboxyanhydrides are capable of activating nucleotides have indeed been reported (Pascal et al. 2005; Biron et al. 2005). The driving forces for the emergence of life would anyway include the availability of energy for the self-organizing system in quantity and quality sufficient to feed the metabolism and especially to deliver quanta of energy able to provoke the formation of the key activated intermediates needed for the amplification of the whole network. Lastly, these observations are consistent with the idea that there is no fundamental difference in the driving force that was responsible for the emergence of the first features of life and its further evolution through the Darwinian process (Pross 2009).
In present day living organisms, pyrophosphate hydrolysis is used to drive aminoacyl adenylate formation to completion so that the later takes advantage of the free energy corresponding to the hydrolysis of both phosphoanhydride bonds of ATP. But a similar prebiotic (or early biological) adenylating pathway seems highly unlikely since it would have required a pyrophosphatase (or a chemical analogue) efficient for pyrophosphate hydrolysis while remaining completely devoid of activity towards the structurally similar phosphoanhydride bonds of ATP.
This work was supported by the Interdisciplinary Program of the CNRS “Origines des Planètes et de la Vie” and by the European COST action CM0703 "Systems Chemistry".
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