The Pigment World: Life's Origins as Photon-Dissipating Pigments.

Many of the fundamental molecules of life share extraordinary pigment-like optical properties in the long-wavelength UV-C spectral region. These include strong photon absorption and rapid (sub-pico-second) dissipation of the induced electronic excitation energy into heat through peaked conical intersections. These properties have been attributed to a "natural selection" of molecules resistant to the dangerous UV-C light incident on Earth's surface during the Archean. In contrast, the "thermodynamic dissipation theory for the origin of life" argues that, far from being detrimental, UV-C light was, in fact, the thermodynamic potential driving the dissipative structuring of life at its origin. The optical properties were thus the thermodynamic "design goals" of microscopic dissipative structuring of organic UV-C pigments, today known as the "fundamental molecules of life", from common precursors under this light. This "UV-C Pigment World" evolved towards greater solar photon dissipation through more complex dissipative structuring pathways, eventually producing visible pigments to dissipate less energetic, but higher intensity, visible photons up to wavelengths of the "red edge". The propagation and dispersal of organic pigments, catalyzed by animals, and their coupling with abiotic dissipative processes, such as the water cycle, culminated in the apex photon dissipative structure, today's biosphere.

Inducing Homochirality Through Intermediary Catalytic Species: A Stochastic Approach.

A new chiral amplification mechanism based on a stochastic approach is proposed. The mechanism includes five different chemical species, an achiral substrate (A), two chiral forms (L, D), and two intermediary species (LA, DA). The process occurs within a small, semipermeable compartment that can be diffusively coupled with the outside environment. The study considers two alternative primary sources for chiral species within the compartment, one chemical and the other diffusive. As a remarkable fact, the chiral amplification process occurs due to stochastic fluctuations of an intermediary catalytic species (LA, DA) produced in situ, given the interaction of the chiral species with the achiral substrate. The net process includes two different steps: the synthesis of the catalyst (LA and DA) and the catalytic production of new chiral species from the substrate. Stochastic simulations show that proper parameterization can induce a robust chiral state within the compartment regardless of whether the system is open or closed. We also show how an increase in the non-catalytic production of chiral species tends to negatively impact the homochirality degree of the system. By its conception, the proposed mechanism suggests a deeper connection with how most biochemical processes occur in living beings, a fact that could open new avenues for studying this fascinating phenomenon.

The Non-Equilibrium Thermodynamics of Natural Selection: From Molecules to the Biosphere.

Evolutionary theory suggests that the origin, persistence, and evolution of biology is driven by the "natural selection" of characteristics improving the differential reproductive success of the organism in the given environment. The theory, however, lacks physical foundation, and, therefore, at best, can only be considered a heuristic narrative, of some utility for assimilating the biological and paleontological data at the level of the organism. On deeper analysis, it becomes apparent that this narrative is plagued with problems and paradoxes. Alternatively, non-equilibrium thermodynamic theory, derived from physical law, provides a physical foundation for describing material interaction with its environment at all scales. Here we describe a "natural thermodynamic selection" of characteristics of structures (or processes), based stochastically on increases in the global rate of dissipation of the prevailing solar spectrum. Different mechanisms of thermodynamic selection are delineated for the different biotic-abiotic levels, from the molecular level at the origin of life, up to the level of the present biosphere with non-linear coupling of biotic and abiotic processes. At the levels of the organism and the biosphere, the non-equilibrium thermodynamic description of evolution resembles, respectively, the Darwinian and Gaia descriptions, although the underlying mechanisms and the objective function of selection are fundamentally very different.

Protective Effects of Halite to Vacuum and Vacuum-Ultraviolet Radiation: A Potential Scenario During a Young Sun Superflare.

Halite (NaCl mineral) has exhibited the potential to preserve microorganisms for millions of years on Earth. This mineral was also identified on Mars and in meteorites. In this study, we investigated the potential of halite crystals to protect microbial life-forms on the surface of an airless body (e.g., meteorite), for instance, during a lithopanspermia process (interplanetary travel step) in the early Solar System. To investigate the effect of the radiation of the young Sun on microorganisms, we performed extensive simulation experiments by employing a synchrotron facility. We focused on two exposure conditions: vacuum (low Earth orbit, 10-4 Pa) and vacuum-ultraviolet (VUV) radiation (range 57.6-124 nm, flux 7.14 W/m2), with the latter representing an extreme scenario with high VUV fluxes comparable to the amount of radiation of a stellar superflare from the young Sun. The stellar VUV parameters were estimated by using the very well-studied solar analog of the young Sun, κ1 Cet. To evaluate the protective effects of halite, we entrapped a halophilic archaeon (Haloferax volcanii) and a non-halophilic bacterium (Deinococcus radiodurans) in laboratory-grown halite. Control groups were cells entrapped in salt crystals (mixtures of different salts and NaCl) and non-trapped (naked) cells, respectively. All groups were exposed either to vacuum alone or to vacuum plus VUV. Our results demonstrate that halite can serve as protection against vacuum and VUV radiation, regardless of the type of microorganism. In addition, we found that the protection is higher than provided by crystals obtained from mixtures of salts. This extends the protective effects of halite documented in previous studies and reinforces the possibility to consider the crystals of this mineral as potential preservation structures in airless bodies or as vehicles for the interplanetary transfer of microorganisms.

A scenario for the origin of life: Volume regulation by bacteriorhodopsin required extremely voltage sensitive Na-channels and very selective K-channels.

The osmotic activity produced by internal, non-permeable, anionic nucleic acids and metabolites causes a persistent and life-threatening cell swelling, or cellular edema, produced by the Gibbs-Donnan effect. This evolutionary-critical osmotic challenge must have been resolved by LUCA or its ancestors, but we lack a cell-physiology look into the biophysical constraints to the solutions. Like mycoplasma, early cells conceivably preserved their volume with Cl- , Na+ , and K+ -channels, Na+ /H+ -exchangers, and a light-dependent bacteriorhodopsin-like H+ -pump. Here, I simulated protocells having these ionic-permeabilities and inhabiting an oceanic pond before the Great-Oxygenation-Event. Protocells showed better volume control and stable resting potentials at lower external pH and higher temperatures, favoring a certain type of extremophile life. Prevention of Na+ -influx at night, with low bacteriorhodopsin activity, required deep shutdown of highly voltage-sensitive Na+ -channels and extremely selective K+ -channels, two conserved features essential for modern neuronal encoding. The Gibbs-Donnan effect universality implies that extraterrestrial cells, if they exist, may reveal similar volume-controlling mechanisms.

Evolutionary timeline of a modeled cell.

A theoretical study of cell evolution is presented here. By using a toolbox containing an intracellular catalytic reaction network model and a mutation-selection process, four distinct phases of self-organization were unveiled. First, the nutrients prevail as the central substrate of the chemical reactions. Second, the cell becomes a small-world. Third, a highly connected core component emerges, concurrently with the nutrient carriers becoming the central product of reactions. Finally, the cell reaches a steady configuration where the concentrations of the core chemical species are described by Zipf's law.

Prebiotic chemical refugia: multifaceted scenario for the formation of biomolecules in primitive Earth.

The origin of life was a cosmic event happened on primitive Earth. A critical problem to better understand the origins of life in Earth is the search for chemical scenarios on which the basic building blocks of biological molecules could be produced. Classic works in pre-biotic chemistry frequently considered early Earth as an homogeneous atmosphere constituted by chemical elements such as methane (CH4), ammonia (NH3), water (H2O), hydrogen (H2) and hydrogen sulfide (H2S). Under that scenario, Stanley Miller was capable to produce amino acids and solved the question about the abiotic origin of proteins. Conversely, the origin of nucleic acids has tricked scientists for decades once nucleotides are complex, though necessary molecules to allow the existence of life. Here we review possible chemical scenarios that allowed not only the formation of nucleotides but also other significant biomolecules. We aim to provide a theoretical solution for the origin of biomolecules at specific sites named "Prebiotic Chemical Refugia." Prebiotic chemical refugium should therefore be understood as a geographic site in prebiotic Earth on which certain chemical elements were accumulated in higher proportion than expected, facilitating the production of basic building blocks for biomolecules. This higher proportion should not be understood as static, but dynamic; once the physicochemical conditions of our planet changed periodically. These different concentration of elements, together with geochemical and astronomical changes along days, synodic months and years provided somewhat periodic changes in temperature, pressure, electromagnetic fields, and conditions of humidity, among other features. Recent and classic works suggesting most likely prebiotic refugia on which the main building blocks for biological molecules might be accumulated are reviewed and discussed.

Dissipative Photochemical Abiogenesis of the Purines.

We have proposed that the abiogenesis of life around the beginning of the Archean may have been an example of "spontaneous" microscopic dissipative structuring of UV-C pigments under the prevailing surface ultraviolet solar spectrum. The thermodynamic function of these Archean pigments (the "fundamental molecules of life"), as for the visible pigments of today, was to dissipate the incident solar light into heat. We have previously described the non-equilibrium thermodynamics and the photochemical mechanisms which may have been involved in the dissipative structuring of the purines adenine and hypoxanthine from the common precursor molecules of hydrogen cyanide and water under this UV light. In this article, we extend our analysis to include the production of the other two important purines, guanine and xanthine. The photochemical reactions are presumed to occur within a fatty acid vesicle floating on a hot (∼80 ∘C) neutral pH ocean surface exposed to the prevailing UV-C light. Reaction-diffusion equations are resolved under different environmental conditions. Significant amounts of adenine (∼10-5 M) and guanine (∼10-6 M) are obtained within 60 Archean days, starting from realistic concentrations of the precursors hydrogen cyanide and cyanogen (∼10-5 M).

Schrödinger and the Possible Existence of Different Types of Life.

Eighty years ago, Nobel Prize-winner physicist Erwin Schrödinger gave three lectures in Dublin's Trinity College, titled What is Life? The physical aspect of the living cell to explain life in terms of the chemistry and physics laws. Life definitions rely on the cellular theory, which poses in the first place that life is made up of cells. The recent discovery of giant viruses, along with the development of synthetic cells at the beginning of century 21st, has challenged the current idea of what life is. Thus, rather than having arrived at a close answer to Schrödinger's question, modern biology has touched down at a novel scenario in which several types of life-as opposed to only one-actually might exist on Earth and possibly the Universe. Eighty years after the Dublin lectures, the Schrödinger question could be: "What are lives"?

A Photon Force and Flow for Dissipative Structuring: Application to Pigments, Plants and Ecosystems.

Through a modern derivation of Planck's formula for the entropy of an arbitrary beam of photons, we derive a general expression for entropy production due to the irreversible process of the absorption of an arbitrary incident photon spectrum in material and its dissipation into an infrared-shifted grey-body emitted spectrum, with the rest being reflected or transmitted. Employing the framework of Classical Irreversible Thermodynamic theory, we define the generalized thermodynamic flow as the flow of photons from the incident beam into the material and the generalized thermodynamic force is, then, the entropy production divided by the photon flow, which is the entropy production per unit photon at a given wavelength. We compare the entropy production of different inorganic and organic materials (water, desert, leaves and forests) under sunlight and show that organic materials are the greater entropy-producing materials. Intriguingly, plant and phytoplankton pigments (including chlorophyll) reach peak absorption exactly where entropy production through photon dissipation is maximal for our solar spectrum 430<λ<550 nm, while photosynthetic efficiency is maximal between 600 and 700 nm. These results suggest that the evolution of pigments, plants and ecosystems has been towards optimizing entropy production, rather than photosynthesis. We propose using the wavelength dependence of global entropy production as a biosignature for discovering life on planets of other stars.

Prebiotic Aggregates (Tissues) Emerging from Reaction-Diffusion: Formation Time, Configuration Entropy and Optimal Spatial Dimension.

For the formation of a proto-tissue, rather than a protocell, the use of reactant dynamics in a finite spatial region is considered. The framework is established on the basic concepts of replication, diversity, and heredity. Heredity, in the sense of the continuity of information and alike traits, is characterized by the number of equivalent patterns conferring viability against selection processes. In the case of structural parameters and the diffusion coefficient of ribonucleic acid, the formation time ranges between a few years to some decades, depending on the spatial dimension (fractional or not). As long as equivalent patterns exist, the configuration entropy of proto-tissues can be defined and used as a practical tool. Consequently, the maximal diversity and weak fluctuations, for which proto-tissues can develop, occur at the spatial dimension 2.5.

Experimental Approaches for Testing the Hypothesis of the Emergence of Life at Submarine Alkaline Vents.

Since the pioneering experimental work performed by Urey and Miller around 70 years ago, several experimental works have been developed for approaching the question of the origin of life based on very few well-constructed hypotheses. In recent years, attention has been drawn to the so-called alkaline hydrothermal vents model (AHV model) for the emergence of life. Since the first works, perspectives from complexity sciences, bioenergetics and thermodynamics have been incorporated into the model. Consequently, a high number of experimental works from the model using several tools have been developed. In this review, we present the key concepts that provide a background for the AHV model and then analyze the experimental approaches that were motivated by it. Experimental tools based on hydrothermal reactors, microfluidics and chemical gardens were used for simulating the environments of early AHVs on the Hadean Earth (~4.0 Ga). In addition, it is noteworthy that several works used techniques from electrochemistry to investigate phenomena in the vent-ocean interface for early AHVs. Their results provided important parameters and details that are used for the evaluation of the plausibility of the AHV model, and for the enhancement of it.

From RNA to DNA: Insights about the transition of informational molecule in the biological systems based on the structural proximity between the polymerases.

Structural relations in an evolutionary context of polymerases is crucial to gain insights into the transition from an RNA world to a Ribonucleoprotein world. Herein, we present a structural proximity tree for the polymerases, from which we observe that the enzymes that have RNA as substrate are more homogeneous than the group with DNA as substrate. The homogeneity observed in enzymes with RNA as a substrate, may be because they performed all steps in information processing. In this sense, the emergence of the DNA molecule posed new challenges to the biological systems, where several parts of the informational flow were individualized by the emergence of enzymes for each step. From the data presented, we propose a polymerase diversification model, in which we have RNA-dependent RNA polymerases as an ancestor and all other polymerases diverged directly from this group by a radiation process.

The Dissipative Photochemical Origin of Life: UVC Abiogenesis of Adenine.

The non-equilibrium thermodynamics and the photochemical reaction mechanisms are described which may have been involved in the dissipative structuring, proliferation and complexation of the fundamental molecules of life from simpler and more common precursors under the UVC photon flux prevalent at the Earth's surface at the origin of life. Dissipative structuring of the fundamental molecules is evidenced by their strong and broad wavelength absorption bands in the UVC and rapid radiationless deexcitation. Proliferation arises from the auto- and cross-catalytic nature of the intermediate products. Inherent non-linearity gives rise to numerous stationary states permitting the system to evolve, on amplification of a fluctuation, towards concentration profiles providing generally greater photon dissipation through a thermodynamic selection of dissipative efficacy. An example is given of photochemical dissipative abiogenesis of adenine from the precursor HCN in water solvent within a fatty acid vesicle floating on a hot ocean surface and driven far from equilibrium by the incident UVC light. The kinetic equations for the photochemical reactions with diffusion are resolved under different environmental conditions and the results analyzed within the framework of non-linear Classical Irreversible Thermodynamic theory.

The Theory of Chemical Symbiosis: A Margulian View for the Emergence of Biological Systems (Origin of Life).

The theory of chemical symbiosis (TCS) suggests that biological systems started with the collaboration of two polymeric molecules existing in early Earth: nucleic acids and peptides. Chemical symbiosis emerged when RNA-like nucleic acid polymers happened to fold into 3D structures capable to bind amino acids together, forming a proto peptidyl-transferase center. This folding catalyzed the formation of quasi-random small peptides, some of them capable to bind this ribozyme structure back and starting to form an initial layer that would produce the larger subunit of the ribosome by accretion. TCS suggests that there is no chicken-and-egg problem into the emergence of biological systems as RNAs and peptides were of equal importance to the origin of life. Life has initially emerged when these two macromolecules started to interact in molecular symbiosis. Further, we suggest that life evolved into progenotes and cells due to the emergence of new layers of symbiosis. Mutualism is the strongest force in biology, capable to create novelties by emergent principles; on which the whole is bigger than the sum of the parts. TCS aims to apply the Margulian view of biology into the origins of life field.

Photon Dissipation as the Origin of Information Encoding in RNA and DNA.

Ultraviolet light incident on organic material can initiate its spontaneous dissipative structuring into chromophores which can catalyze their own replication. This may have been the case for one of the most ancient of all chromophores dissipating the Archean UVC photon flux, the nucleic acids. Oligos of nucleic acids with affinity to particular amino acids which foment UVC photon dissipation would most efficiently catalyze their own reproduction and thus would have been selected through non-equilibrium thermodynamic imperatives which favor dissipation. Indeed, we show here that those amino acids with characteristics most relevant to fomenting UVC photon dissipation are precisely those with greatest chemical affinity to their codons or anticodons. This could provide a thermodynamic basis for the specificity in the amino acid-nucleic acid interaction and an explanation for the accumulation of information in nucleic acids since this information is relevant to the optimization of dissipation of the externally imposed thermodynamic potentials. The accumulation of information in this manner provides a link between evolution and entropy production.

Natural Radioactive Environments as Sources of Local Disequilibrium for the Emergence of Life.

Certain subterranean environments of Earth have naturally accumulated long-lived radionuclides, such as 238U, 232Th, and 40K, near the presence of liquid water. In these natural radioactive environments, water radiolysis can produce chemical species of biological importance, such as H2. Although the proposal of radioactive decay as an alternative source of energy for living systems has existed for >30 years, this hypothesis gained strength after the recent discovery of a peculiar ecosystem in a gold mine in South Africa, whose existence is dependent on chemical species produced by water radiolysis. In this study, we calculate the chemical disequilibrium generated locally by water radiolysis due to gamma radiation. We then analyze the possible contribution of this disequilibrium for the emergence of life, considering conditions of early Earth and having as reference the alkaline hydrothermal vent theory. Results from our kinetic model point out the similarities between the conditions caused by water radiolysis and those found on alkaline hydrothermal systems. Our model produces a steady increase of pH with time, which favors the formation of a natural electrochemical gradient and the precipitation of minerals with catalytic activity for protometabolism in this aqueous environment. We conclude by describing a possible free-energy conversion mechanism based on protometabolism, which could be a requisite for the emergence of life in Hadean Earth.

The Ancient History of Peptidyl Transferase Center Formation as Told by Conservation and Information Analyses.

The peptidyl transferase center (PTC) is the catalytic center of the ribosome and forms part of the 23S ribosomal RNA. The PTC has been recognized as the earliest ribosomal part and its origins embodied the First Universal Common Ancestor (FUCA). The PTC is frequently assumed to be highly conserved along all living beings. In this work, we posed the following questions: (i) How many 100% conserved bases can be found in the PTC? (ii) Is it possible to identify clusters of informationally linked nucleotides along its sequence? (iii) Can we propose how the PTC was formed? (iv) How does sequence conservation reflect on the secondary and tertiary structures of the PTC? Aiming to answer these questions, all available complete sequences of 23S ribosomal RNA from Bacteria and Archaea deposited on GenBank database were downloaded. Using a sequence bait of 179 bp from the PTC of Thermus termophilus, we performed an optimum pairwise alignment to retrieve the PTC region from 1424 filtered 23S rRNA sequences. These PTC sequences were multiply aligned, and the conserved regions were assigned and observed along the primary, secondary, and tertiary structures. The PTC structure was observed to be more highly conserved close to the adenine located at the catalytical site. Clusters of interrelated, co-evolving nucleotides reinforce previous assumptions that the PTC was formed by the concatenation of proto-tRNAs and important residues responsible for its assembly were identified. The observed sequence variation does not seem to significantly affect the 3D structure of the PTC ribozyme.

Unexpected Thiocyanate Adsorption onto Ferrihydrite Under Prebiotic Chemistry Conditions.

The most crucial role played by minerals was in the preconcentration of biomolecules or precursors of biomolecules in prebiotic seas. If this step had not occurred, molecular evolution would not have occurred. Thiocyanate is an important molecule in the formation of biomolecules as well as a catalyst for prebiotic reactions. The adsorption of thiocyanate onto ferrihydrite was carried out under pH and ion composition conditions in seawater that resembled those of prebiotic Earth. The seawater used in this work had high Mg2+, Ca2+ and SO42- concentrations. The most important result of this work was that ferrihydrite adsorbed thiocyanateata pH value (7.2 ± 0.2) that usually does not adsorb thiocyanate. The high adsorptivity of Mg2+, Ca2+ and SO42-onto ferrihydrite showed that seawater ions can act as carriers of thiocyanate to the ferrihydrite surface, creating a huge outer-sphere complex. Kinetic adsorption and isotherm experiments showed the best fit for the pseudo-second-order model and an activation energy of 23.8 kJ mol-1forthe Langmuir-Freundlich model, respectively. Thermodynamic data showed positive ΔG values, which apparently contradict the adsorption isotherm data and kinetic data that was obtained. The adsorption of thiocyanate onto ferrihydrite could be explained by coupling with the exergonic SO42- adsorption onto ferrihydrite. The FTIR spectra showed no difference between the C≡N stretching peaks of adsorbed thiocyanate and free thiocyanate, corroborating the formation of an outer-sphere complex. All the results demonstrated the importance of the artificial seawater composition for the adsorption of thiocyanate and for understanding prebiotic chemistry.

Viruses as a survival strategy in the armory of life.

Viruses have generally been thought of as infectious agents. New data on mimivirus, however, suggests a reinterpretation of this thought. Earth's biosphere seems to contain many more viruses than previously thought and they are relevant in the maintenance of ecosystems and biodiversity. Viruses are not considered to be alive because they are not free-living entities and do not have cellular units. Current hypotheses indicate that some viruses may have been the result of genomic reduction of cellular life forms. However, new studies relating to the origins of biological systems suggest that viruses could also have originated during the transition from First to the Last Universal Common Ancestor (from FUCA to LUCA). Within this setting, life has been established as chemical informational system and could be interpreted as a macrocode of multiple layers. The first entity to acquire these features was the First Universal Common Ancestor (FUCA) that evolved to an intermediate ancestral that could be named T-LUCA (Transitional-LUCA) and be equated to Woese's concept of progenotes. T-LUCA may have remained as undifferentiated subsystems with viruses-like structures. The net result is that both cellular life forms and viruses shared protein synthesis apparatuses. In short, virus is a strategy of life reached by two paths: T-LUCAs like entities and the reduction of cellular life forms.