Non-equilibrium Thermodynamic Foundations of the Origin of Life

: There is little doubt that life’s origin followed from the known physical and chemical laws 1 of Nature. The most general scientific framework incorporating the laws of Nature and applicable to 2 most known processes to good approximation, is that of thermodynamics and its extensions to treat 3 out-of-equilibrium phenomena. The event of the origin of life should therefore also be amenable to 4 such an analysis. In this paper, I describe the non-equilibrium thermodynamic foundations of the 5 origin of life for the non-expert. This “Thermodynamic Dissipation Theory for the Origin of Life” is 6 founded on Classical Irreversible Thermodynamic theory developed by Lars Onsager, Ilya Prigogine, 7 and coworkers. 8

their template directed reproduction overnight with the aid of transition metal ion catalysts. In section 145 3.6 I describe how the association between DNA or RNA codons (or anticodons) and their cognate 146 amino acids formed through dissipative structuring because this led to increased photon dissipation 147 for the DNA/RNA-amino acid complex. Finally, in section 3.7, I describe how homochirality of the 148 fundamental molecules would have arisen naturally if the UVTAR mechanism for denaturing RNA 149 and DNA was operating asymmetrically (morning/afternoon) on the Archean ocean surface.

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This apparent puzzle persists even today, especially among those who prefer that the origin of life 160 remain a mystery inaccessible to human comprehension, and thereby best ascribable to a omnipotent 161 supernatural being. Many non-specialists also incorrectly assume that the second law is applicable to 162 all systems, life included. However, Boltzmann, even in 1886, realized that systems can be either isolated 163 (no flow of energy or matter, or work performed, over the boundary of the system), closed (only energy multiple dynamical meta-stable states for a system, including states in which there appeared to be 181 a spontaneous symmetry breaking and associated structuring of material in space and time within 182 the system. As Boltzmann had first observed, such a structured system had the particular property of 183 inevitably increasing the rate of the spread of the conserved quantities (energy, momentum, angular 184 momentum, charge) over the microscopic degrees of freedom of the environment, or, in other words, 185 increasing the rate of dissipation of the imposed external force (rate of entropy production). Prigogine 186 called these structures dissipative structures and showed that they arise only far from equilibrium, 187 where large external forces took the system into the non-linear regime. 188 The realization that non-linear systems had multiple dynamical meta-stable states, unlike the 189 one static equilibrium state, meant that the system, responding to perturbation, could evolve over 190 these states, and the direction of evolution for many biological systems tended towards states with 191 greater entropy production (greater rate of distribution of the conserved quantities of nature over more 192 microscopic degrees of freedom). A deep understanding of many complex phenomena in Nature,193 including meteorological systems, turbulence, and the vitality of life, thus began to emerge.

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In summary, isolated systems always moved towards the equilibrium state, of which there is, 195 always, only one, and this state corresponds to a maximum of entropy, i.e. to a maximum probability 196 distribution of the conserved quantities over all the microscopic degrees of freedom. No enduring 197 macroscopic dynamics or vitality is allowed for isolated systems, they inevitably decay towards a 198 static equilibrium state since any dynamics would imply that the conserved quantity of energy or 199 momentum was not distributed with maximal probability over all microscopic degrees of freedom.

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Open systems like life, or even closed systems (only work and energy flow over the system, but no 201 mass flow) could, however, evolve to dynamical meta-stable states of which there could be many, 202 and the system could evolve from one such state to another depending on its initial conditions and 203 subsequent perturbations.

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In the process of this evolution, the open system could become more organized (structuring not 205 only in space, but also in time, implying a macroscopic process with dynamic vitality). Even more 206 interesting, this structuring, in the case of non-linear systems with positive feedback, provided greater 207 efficacy for the distribution of the conserved quantities over more microscopic degrees of freedom of 208 the environment, i.e. greater entropy production rates. For this reason, these structures were given

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The proposed thermodynamic dissipation theory suggests that life arose as dissipative structuring 228 of UVC pigments on the surface of Earth's oceans to augment the global entropy production through 229 photon dissipation. In fact, any dissipative structure, also known as an "irreversible process," originates 230 and persists for only this fundamental reason; to distribute the conserved quantities of nature over 231 ever more microscopic degrees of freedom, i.e. to produce entropy.

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Currently, a large amount of living material, known as phytoplankton (microorganisms such as 233 cyanobacteria and diatoms), float on the surface of Earth's oceans. Besides these, there are also many 234 viruses and free floating RNA and DNA fragments, pigments, lipids, and other organic compounds

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The extremely rapid de-excitation of the fundamental molecules also means, by the Heisenberg 306 uncertainty principle ∆E∆t >h, that they also absorb over a wide wavelength region (i.e. ∆E is large 307 since ∆t is small). As we will see, this has important consequences for the "thermodynamic selection" 308 of these molecules over other possible configurations. Ga and until at least 2.9 Ga (curves black and red respectively) during the Archean. CO 2 and probably some H 2 S were responsible for absorption at wavelengths shorter than ∼ 205 nm and atmospheric aldehydes (comon photochemical products of CO 2 and water) absorbed between about 285 and 310 nm [29], approximately corresponding to the UVB region. Around 2.2 Ga (yellow curve), UVC light at Earth's surface had been extinguished by oxygen and ozone resulting from organisms performing oxygenic photosynthesis. The green curve corresponds to the present surface spectrum. Energy fluxes are for the sun at the zenith. The names of the fundamental molecules of life, nucleic acids (black), amino acids (green), fatty acids (violet), sugars (brown), vitamins, co-enzymes and co-factors (blue), and pigments (red) are plotted at their wavelengths of maximal absorption (the font size of the letter roughly corresponds to the relative size of their molar extinction coefficient, i.e. how well they absorb). Note how closely these wavelengths of maximum absorption coincide with the Archean UV surface spectrum. Adapted from Michaelian and Simeonov [14].

Figure 2. Conical Intersection (CI) for adenine (one of the nucelobases)
showing the degeneracy of the electronic excited state with the electronic ground state after a UVC photon absorption event (blue arrow) which induces a nuclear coordinate deformation, known as pyrimidilization, from its original structure in the Franck-Condon (FC) region. In this deformed state, the vibrational states of the excited potential energy surface coincide in a region (CI) with the vibrational states on the ground state. Conical intersections provide rapid (sub-picosecond) dissipation of the original electronic excitation energy into heat. The quantum efficiency (q) for this dissipative route is very large, making adenine photochemically stable but, more importantly, very efficient at photon dissipation.   able to obtain a copious production of the purine nucleobase adenine with HCN in warm water. The 359 fact that many of these fundamental molecules have now also been found in meteorites, on the surface 360 of comets, and even in the very cold interstellar gas and dust clouds, hints at the utility of UV light 361 as a free energy source for their production under a myriad of different physical conditions. There 362 remains, of course, an important question to resolve as to which chemical or photochemical routes 363 were the actual routes that brought these first molecules to the surface of Earth.

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An important clue to answering this question was given in the Introduction in that life is much 365 more than a simple collection of fundamental molecules arranged in a particular pattern. Life manifests 366 a vitality as seen in macroscopic dynamical processes such as; proliferation, mobility, metabolism, 367 homeostasis, increases in complexity, and the ability to evolve and adapt to different environments.  states. This also means that natural fluctuations in the environment, or within the system itself, could 384 cause the system to leave its initial state and evolve towards those more stable states (configurations) 385 that produce greater dissipation of the free energy incident from the environment.

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An example of one such system in which two stable states exist for the system under the same This is, therefore, the state that we should expect to encounter in nature most frequently, and, in fact, 402 experiment verifies this. Figure 3. The Bénard cell. The system consists of a hot lower plate and a cold upper plate which sandwiches a liquid and the whole system is under the force of gravity. The onset of self-organization (structuring of material in space and time) occurs as a result of an external force (temperature gradient) imposed over the system, and a non-linear relation between the flow of heat and the temperature gradient. The left part of the figure 3 (a) describes the linear situation for the relation between the force (temperature gradient) and the flow (heat flow) when the temperature difference over the system is small, below some critical value ∆T c and results in a homogeneous system (no spatial symmetry breaking) and there exists only conduction of heat. The right part of (a) describes the non-linear situation when the temperature difference between the two plates is greater than some critical value ∆T c for which convection cells spontaneously arise (Bénard cells) and spatial symmetry breaking occurs. There are two stationary states allowed for this system once the critical temperature gradient is reached; one with the hot liquid coming up through the center, and the other with the hot liquid coming up around the edges of the approximately hexagonal cells. The greater entropy producing d i S/dt state is the one with the hot liquid coming up through the center of the cells and this is the state of greater stability and thus the most probable given internal and external fluctuations of the material flow and temperature. This is shown in the bifurcation diagram (b) which describes the direction taken by the system in terms of entropy production as given by the arrows. The general trend is towards greater entropy production.
The same dynamics, we argue, is true for the case of microscopic dissipative structuring of the fundamental UV-C dissipating molecules, and this, through the donor-acceptor mechanism, would 508 have led to a greater dissipating complex than the sum of its parts and so be thermodynamically 509 selected. Besides leading to greater dissipation, since the affinity of the donor chromophore molecule 510 to the RNA or DNA acceptor is selective to only particular codons, then this dissipation-replication 511 mechanism would also have led to information accumulation in RNA and DNA (information for 512 optimizing dissipation) and to a thermodynamic advantage, in terms of photon dissipation, to evolving 513 a faithful replication mechanism [22].

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This process is depicted in figure 5 and is similar to a technique commonly used in the laboratory 553 to amplify (multiply) DNA known as the Polymerase Chain Reaction, or, simply PCR. Our process, 554 however, uses the absorption of UVC light rather than heat to denature. This mechanism of denaturing, 555 UVTAR, is not hypothetical, we have shown experimentally that it occurs for DNA and we have 556 measured its temperature dependence [13]. , would have had a greater chance of denaturing during daylight hours as the ocean surface temperature cooled throughout the Archean, and could therefore be replicated overnight. This selection based on greater photon dissipation we have termed "thermodynamic selection" [9,10,15,23]. The important aspect of this auto-catalytic mechanism is that replication is tied to photon dissipation, providing a thermodynamic imperative for proliferation. Taken with permission from [22]. It is therefore probable that the first information encoded in the RNA and DNA was that of the 565 codons or anti-codons corresponding to these amino acids which promote dissipation. A greater 566 photon dissipation rate would lead to a greater denaturing rate for the DNA or RNA strands that 567 coded for these amino acids and thus to their greater replication rate, especially as the seas cooled 568 throughout the Archean. Such thermodynamic selection at the molecular complex level then leads to 569 the evolution of ever greater dissipative systems.

Evolution
Dissipative structuring under light, as the fundamental creative force in biology, appears to have 571 been ongoing, from the initial dissipation at the UVC wavelengths of the Archean by the fundamental 572 molecules of life, to the dissipation of wavelengths up to the red edge (∼ 700 nm) by the organic 573 pigments of today [9,10,14]. Beyond the red edge, starting at about 1200 nm, water in the ocean surface 574 microlayer absorbs strongly and dissipates photons into heat efficiently. There is, therefore, still a 575 wavelength region between 700 and 1200 nm which remains to be conquered by future evolution of 576 pigments. The simultaneous coupling of biotic with abiotic irreversible processes, such as the water 577 cycle and ocean and air currents, culminating in an efficient global dissipating system known as the 578 biosphere, increases further the efficacy of solar photon dissipation into the far infrared much beyond 579 1200 nm [9,11,12]. of this presentation simply because of lack of space, but the interested reader is encouraged to 707 explore the following references in which the most important details are more thoroughly considered;