An Aristotelian account of minimal chemical life

This paper addresses the open philosophical and scientific problem of explaining and defining life. This problem is controversial, and there is nothing approaching a consensus about what life is. This raises a philosophical meta-question: Why is life so controversial and so difficult to define? This paper proposes that we can attribute a significant part of the controversy over life to use of a Cartesian approach to explaining life, which seeks necessary and sufficient conditions for being an individual living organism, out of the context of other organisms and the abiotic environment. The Cartesian approach contrasts with an Aristotelian approach to explaining life, which considers life only in the whole context in which it actually exists, looks at the characteristic phenomena involving actual life, and seeks the deepest and most unified explanation for those phenomena. The phenomena of life might be difficult to delimit precisely, but it certainly includes life's characteristic hallmarks, borderline cases, and puzzles. The Program-Metabolism-Container (PMC) model construes minimal chemical life as a functionally integrated triad of chemical systems, which are identified as the Program, Metabolism, and Container. Rasmussen diagrams precisely depict the functional definition of minimal chemical life. The PMC model illustrates the Aristotelian approach to life, because it explains eight of life's hallmarks, one of life's borderline cases (the virus), and two of life's puzzles.     

The definition of life: a brief history of an elusive scientific endeavor

In spite of the spectacular developments in our understanding of the molecular basis that underlies biological phenomena, we still lack a generally agreed-upon definition of life, but this is not for want of trying. Life is an empirical concept; and, as suggested by the many unsuccessful efforts to define it, this task is likely to remain, at best, a work in progress. Although phenomenological characterizations of life are feasible, a precise definition of life remains an elusive intellectual endeavor. This is not surprising: as Nietszche once wrote, there are concepts that can be defined, whereas others only have a history. The purpose of this essay is to discuss some of the manifold (and often unsatisfactory) definitions of life that have been attempted from different intellectual and scientific perspectives and reflect, at least in part, the key role that historical frameworks play. Although some efforts have been more fruitful, the lack of an all-embracing, generally agreed-upon definition of life sometimes gives the impression that what is meant by life's origin is defined in somewhat imprecise terms and that several entirely different questions are often confused. The many attempts made to reduce the nature of living systems to a single living compound imply that life can be so well defined that the exact point at which it started can be established with the sudden appearance of the first replicating molecule. On the other hand, if the emergence of life is seen as the stepwise (but not necessarily slow) evolutionary transition between the non-living and the living, then it may be meaningless to draw a strict line between them.     

The effect of a strong stellar flare on the atmospheric chemistry of an earth-like planet orbiting an M dwarf

Main sequence M stars pose an interesting problem for astrobiology: their abundance in our galaxy makes them likely targets in the hunt for habitable planets, but their strong chromospheric activity produces high-energy radiation and charged particles that may be detrimental to life. We studied the impact of the 1985 April 12 flare from the M dwarf AD Leonis (AD Leo), simulating the effects from both UV radiation and protons on the atmospheric chemistry of a hypothetical, Earth-like planet located within its habitable zone. Based on observations of solar proton events and the Neupert effect, we estimated a proton flux associated with the flare of 5.9?×?10? protons cm?2 sr?1 s?1 for particles with energies >10?MeV. Then we calculated the abundance of nitrogen oxides produced by the flare by scaling the production of these compounds during a large solar proton event called the Carrington event. The simulations were performed with a 1-D photochemical model coupled to a 1-D radiative/convective model. Our results indicate that the UV radiation emitted during the flare does not produce a significant change in the ozone column depth of the planet. When the action of protons is included, the ozone depletion reaches a maximum of 94% two years after the flare for a planet with no magnetic field. At the peak of the flare, the calculated UV fluxes that reach the surface, in the wavelength ranges that are damaging for life, exceed those received on Earth during less than 100?s. Therefore, flares may not present a direct hazard for life on the surface of an orbiting habitable planet. Given that AD Leo is one of the most magnetically active M dwarfs known, this conclusion should apply to planets around other M dwarfs with lower levels of chromospheric activity.     

Magnetotactic bacteria on Earth and on Mars

Continued interest in the possibility of evidence for life in the ALH84001 Martian meteorite has focused on the magnetite crystals. This review is structured around three related questions: is the magnetite in ALH84001 of biological or non-biological origin, or a mixture of both? does magnetite on Earth provide insight to the plausibility of biogenic magnetite on Mars? could magnetotaxis have developed on Mars? There are credible arguments for both the biological and non-biological origin of the magnetite in ALH84001, and we suggest that more studies of ALH84001, extensive laboratory simulations of non-biological magnetite formation, as well as further studies of magnetotactic bacteria on Earth will be required to further address this question. Magnetite grains produced by bacteria could provide one of the few inorganic traces of past bacterial life on Mars that could be recovered from surface soils and sediments. If there was biogenic magnetite on Mars in sufficient abundance to leave fossil remains in the volcanic rocks of ALH84001, then it is likely that better-preserved magnetite will be found in sedimentary deposits on Mars. Deposits in ancient lakebeds could contain well-preserved chains of magnetite clearly indicating a biogenic origin.     

A combinatorial approach to biochemical space: description and application to the redox distribution of metabolism

Redox chemistry is central to life on Earth. It is well known that life uses redox chemistry to capture energy from environmental chemical energy gradients. Here, we propose that a second use of redox chemistry, related to building biomass from environmental carbon, is equally important to life. We apply a method based on chemical structure to evaluate the redox range of different groups of terrestrial biochemicals, and find that they are consistently of intermediate redox range. We hypothesize the common intermediate range is related to the chemical space required for the selection of a consistent set of metabolites. We apply a computational method to show that the redox range of the chemical space shows the same restricted redox range as the biochemicals that are selected from that space. By contrast, the carbon from which life is composed is available in the environment only as fully oxidized or reduced species. We therefore argue that redox chemistry is essential to life for assembling biochemicals for biomass building. This biomass-building reason for life to require redox chemistry is in addition (and in contrast) to life's use of redox chemistry to capture energy. Life's use of redox chemistry for biomass capture will generate chemical by-products-that is, biosignature gases-that are not in redox equilibrium with life's environment. These potential biosignature gases may differ from energy-capture redox biosignatures.     

Chaotic exchange of solid material between planetary systems: implications for lithopanspermia

Abstract We examined a low-energy mechanism for the transfer of meteoroids between two planetary systems embedded in a star cluster using quasi-parabolic orbits of minimal energy. Using Monte Carlo simulations, we found that the exchange of meteoroids could have been significantly more efficient than previously estimated. Our study is relevant to astrobiology, as it addresses whether life on Earth could have been transferred to other planetary systems in the Solar System's birth cluster and whether life on Earth could have been transferred from beyond the Solar System. In the Solar System, the timescale over which solid material was delivered to the region from where it could be transferred via this mechanism likely extended to several hundred million years (as indicated by the 3.8-4.0?Ga epoch of the Late Heavy Bombardment). This timescale could have overlapped with the lifetime of the Solar birth cluster (～100-500?Myr). Therefore, we conclude that lithopanspermia is an open possibility if life had an early start. Adopting parameters from the minimum mass solar nebula, considering a range of planetesimal size distributions derived from observations of asteroids and Kuiper Belt objects and theoretical coagulation models, and taking into account Oort Cloud formation models, we discerned that the expected number of bodies with mass>10?kg that could have been transferred between the Sun and its nearest cluster neighbor could be of the order of 10(14) to 3·10(16), with transfer timescales of tens of millions of years. We estimate that of the order of 3·10(8)·l (km) could potentially be life-bearing, where l is the depth of Earth's crust in kilometers that was ejected as the result of the early bombardment. Key Words: Extrasolar planets-Interplanetary dust-Interstellar meteorites-Lithopanspermia. Astrobiology 12, 754-774.     

Biosignatures of early earths

A major goal of NASA's Origins Program is to find habitable planets around other stars and determine which might harbor life. Determining whether or not an extrasolar planet harbors life requires an understanding of what spectral features (i.e., biosignatures) might result from life's presence. Consideration of potential biosignatures has tended to focus on spectral features of gases in Earth's modern atmosphere, particularly ozone, the photolytic product of biogenically produced molecular oxygen. But life existed on Earth for about 1(1/2) billion years before the buildup of atmospheric oxygen. Inferred characteristics of Earth's earliest biosphere and studies of modern microbial ecosystems that share some of those characteristics suggest that organosulfur compounds, particularly methanethiol (CH(3)SH, the sulfur analog of methanol), may have been biogenic products on early Earth. Similar production could take place on extrasolar Earth-like planets whose biota share functional chemical characteristics with Earth life. Since methanethiol and related organosulfur compounds (as well as carbon dioxide) absorb at wavelengths near or overlapping the 9.6-microm band of ozone, there is potential ambiguity in interpreting a feature around this wavelength in an extrasolar planet spectrum.     

FeS/S/FeS(2) redox system and its oxidoreductase-like chemistry in the iron-sulfur world

The iron-sulfur world (ISW) theory is an intriguing prediction regarding the origin of life on early Earth. It hypothesizes that life arose as a geochemical process from inorganic starting materials on the surface of sulfide minerals in the vicinity of deep-sea hot springs. During the last two decades, many experimental studies have been carried out on this topic, and some interesting results have been achieved. Among them, however, the processes of carbon/nitrogen fixation and biomolecular assembly on the mineral surface have received an inordinate amount of attention. To the present, an abiotic model for the oxidation-reduction of intermediates participating in metabolic pathways has been ignored. We examined the oxidation-reduction effect of a prebiotic FeS/S/FeS(2) redox system on the interconversion between several pairs of α-hydroxy acids and α-keto acids (i.e., lactate/pyruvate, malate/oxaloacetate, and glycolate/glyoxylate). We found that, in the absence of FeS, elemental sulfur (S) oxidized α-hydroxy acids to form corresponding keto acids only at a temperature higher than its melting point (113°C); in the presence of FeS, such reactions occurred more efficiently through a coupled reaction mechanism, even at a temperature below the phase transition point of S. On the other hand, FeS was shown to have the capacity to reversibly reduce the keto acids. Such an oxidoreductase-like chemistry of the FeS/S/FeS(2) redox system suggests that it can determine the redox homeostasis of metabolic intermediates in the early evolutionary phase of life. The results provide a possible pathway for the development of primordial redox biochemistry in the iron-sulfur world. Key Words: Iron-sulfur world-FeS/S/FeS(2) redox system-Oxidoreductase-like chemistry. Astrobiology 11, 471-476.     

The first cell membranes

Organic compounds are synthesized in the interstellar medium and can be delivered to planetary surfaces such as the early Earth, where they mix with endogenous species. Some of these compounds are amphiphilic, having polar and nonpolar groups on the same molecule. Amphiphilic compounds spontaneously self-assemble into more complex structures such as bimolecular layers, which in turn form closed membranous vesicles. The first forms of cellular life required self-assembled membranes that were likely to have been produced from amphiphilic compounds on the prebiotic Earth. Laboratory simulations show that such vesicles readily encapsulate functional macromolecules, including nucleic acids and polymerases. The goal of future investigations will be to fabricate artificial cells as models of the origin of life.     

Does life's rapid appearance imply a Martian origin?

The hypothesis that life's rapid appearance on Earth justifies the belief that life is widespread in the universe has been investigated mathematically by Lineweaver and Davis (Astrobiology 2002;2:293-304). However, a rapid appearance could also be interpreted as evidence for a nonterrestrial origin. I attempt to quantify the relative probabilities for a non-indigenous versus indigenous origin, on the assumption that biogenesis involves one or more highly improbable steps, using a generalization of Carter's well-known observer-selection argument. The analysis is specifically applied to a Martian origin of life, with subsequent transfer to Earth within impact ejecta. My main result is that the relatively greater probability of a Martian origin rises sharply as a function of the number of difficult steps involved in biogenesis. The actual numerical factor depends on what is assumed about conditions on early Mars, but for a wide range of assumptions a Martian origin of life is decisively favored. By contrast, an extrasolar origin seems unlikely using the same analysis. These results complement those of Lineweaver and Davis.     

Mollusc-microbe mutualisms extend the potential for life in hypersaline systems

Metazoans in extreme environments have evolved mutualisms with microbes that extend the physical and chemical capabilities of both partners. Some of the best examples are bivalve molluscs in evaporite and hypersaline settings. Mollusc tissue is developmentally and evolutionarily amenable to housing vast numbers of symbiotic microbes. Documented benefits to the host are nutritional. Multiple postulated benefits to the microbes are related to optimizing metabolic performance at interfaces, where heterogeneity and steep gradients that cannot be negotiated by microbes can be spanned by larger metazoan hosts. A small cockle, Fragum erugatum, and its photosymbiotic microbes provide a remarkable example of a mutualistic partnership in the hypersaline reaches of Shark Bay, Western Australia. Lucinid bivalves and their endosymbiotic chemolithotrophic bacteria provide examples in which hosts span oxic/anoxic interfaces on behalf of their symbionts at sites of seafloor venting. Multiple lines of evidence underscore the antiquity of mutualisms and suggest that they may have played a significant role in life's first experiments above the prokaryotic grade of complexity. The study of metazoan-microbe mutualisms and their signatures in extreme environments in the geologic record will provide a significant augmentation to microbial models in paleobiology and astrobiology. There are strong potential links between mutualisms and the early history of life on Earth, the persistence of life in extreme environments at times of global crisis and mass extinction, and the possibilities for life elsewhere in the universe.     

Domain evolution and functional diversification of sulfite reductases

Sulfite reductases are key enzymes of assimilatory and dissimilatory sulfur metabolism, which occur in diverse bacterial and archaeal lineages. They share a highly conserved domain "C-X5-C-n-C-X3-C" for binding siroheme and iron-sulfur clusters that facilitate electron transfer to the substrate. For each sulfite reductase cluster, the siroheme-binding domain is positioned slightly differently at the N-terminus of dsrA and dsrB, while in the assimilatory proteins the siroheme domain is located at the C-terminus. Our sequence and phylogenetic analysis of the siroheme-binding domain shows that sulfite reductase sequences diverged from a common ancestor into four separate clusters (aSir, alSir, dsr, and asrC) that are biochemically distinct; each serves a different assimilatory or dissimilatory role in sulfur metabolism. The phylogenetic distribution and functional grouping in sulfite reductase clusters (dsrA and dsrB vs. aSiR, asrC, and alSir) suggest that their functional diversification during evolution may have preceded the bacterial/archaeal divergence.     

Origin of informational polymers and the search for non-terran life: protection of the polymeric state of DNA by phosphate minerals

An in-depth analysis of the effects exerted on the DNA backbone by 25 crystal phosphate minerals is reported. Degradation of DNA oligomers was performed with two different reactions: Hydrolysis following Nucleophilic Degradation (HND), initiated by the nucleophilic addition of formamide on both purine and pyrimidine nucleobases, and Hydrolysis following Nucleophilic Substitution (HNS) carried on by water and starting with the removal of a nondegraded base. A complete panel of effects on the phosphoester bonds, from protection to enhanced instability to absence of interference, is described. These effects differ in the different degradation pathways and in different physical-chemical conditions. The relationship between the hardness of the mineral and its protective ability is discussed. In addition to its interest per se, this study was prompted by the observed catalytic abilities of soluble and mineral phosphates (Saladino et al., 2006c) on the synthetic reactions by formamide. The relevance of these observations in the search for nonterran life is discussed.     

Sequence analysis of trimer isomers formed by montmorillonite catalysis in the reaction of binary monomer mixtures

Oligonucleotides are structurally similar to short RNA strands. Therefore, their formation via non-enzymatic reactions is highly relevant to Gilbert's RNA world scenario (1986) and the origin of life. In laboratory synthesis of oligonucleotides from monomers, it is necessary to remove the water molecules from the reaction medium to shift the equilibrium in favor of oligonucleotide formation, which would have been impossible for reactions that took place in dilute solutions on the early Earth. Model studies designed to address this problem demonstrate that montmorillonite, a phyllosilicate common on Earth and identified on Mars, efficiently catalyzes phosphodiester-bond formation between activated mononucleotides in dilute solutions and produces RNA-like oligomers. The purpose of this study was to examine the sequences and regiospecificity of trimer isomers formed in the reaction of 5'-phosphorimidazolides of adenosine and uridine. Results demonstrated that regiospecificity and sequence specificity observed in the dimer fractions are conserved in their elongation products. With regard to regiospecificity, 61% of the linkages were found to be RNA-like 3',5'-phosphodiester bonds. With regard to sequence specificity, we found that 88% of the linear trimers were hetero-isomers with 61% A-monomer and 39% U-monomer incorporation. These results lend support to Bernal's hypothesis that minerals may have played a significant role in the chemical processes that led to the origin of life by catalyzing the formation of phosphodiester bonds in RNA-like oligomers.     

Eutectic phases in ice facilitate nonenzymatic nucleic acid synthesis

Polymeric compounds similar to oligonucleotides are relevant to the origin of life and particularly to the concept of an RNA world. Although short oligomers of RNA can be synthesized nonenzymatically under laboratory conditions by second-order reactions in concentrated solutions, there is no consensus on how these polymers could have been synthesized de novo on the early Earth from dilute solutions of monomers. To address this question in the context of an RNA world, we have explored ice eutectic phases as a reaction medium. When an aqueous solution freezes, the solutes become concentrated in the spaces between the ice crystals. The increased concentration offsets the effect of the lower temperature and accelerates the reaction. Here we show that in the presence of metal ions in dilute solutions, frozen samples of phosphoimidazolide-activated uridine react within days at -18 degrees C to form oligouridylates up to 11 bases long. Product yields typically exceed 90%, and approximately 30% of the oligomers include one or more 3'-5' linkages. These conditions facilitate not only the notoriously difficult oligouridylate synthesis, but also the oligomerization of activated cytidylate, adenylate, and guanylate. To our knowledge, this represents the first report to indicate that ice matrices on the early Earth may have accelerated certain prebiotic polymerization reactions.     

Abiotic nitrogen fixation on terrestrial planets: reduction of NO to ammonia by FeS

Understanding the abiotic fixation of nitrogen and how such fixation can be a supply of prebiotic nitrogen is critical for understanding both the planetary evolution of, and the potential origin of life on, terrestrial planets. As nitrogen is a biochemically essential element, sources of biochemically accessible nitrogen, especially reduced nitrogen, are critical to prebiotic chemistry and the origin of life. Loss of atmospheric nitrogen can result in loss of the ability to sustain liquid water on a planetary surface, which would impact planetary habitability and hydrological processes that shape the surface. It is known that NO can be photochemically converted through a chain of reactions to form nitrate and nitrite, which can be subsequently reduced to ammonia. Here, we show that NO can also be directly reduced, by FeS, to ammonia. In addition to removing nitrogen from the atmosphere, this reaction is particularly important as a source of reduced nitrogen on an early terrestrial planet. By converting NO directly to ammonia in a single step, ammonia is formed with a higher product yield (~50%) than would be possible through the formation of nitrate/nitrite and subsequent conversion to ammonia. In conjunction with the reduction of NO, there is also a catalytic disproportionation at the mineral surface that converts NO to NO? and N?O. The NO? is then converted to ammonia, while the N?O is released back in the gas phase, which provides an abiotic source of nitrous oxide.     

Key science questions from the second conference on early Mars: geologic, hydrologic, and climatic evolution and the implications for life

In October 2004, more than 130 terrestrial and planetary scientists met in Jackson Hole, WY, to discuss early Mars. The first billion years of martian geologic history is of particular interest because it is a period during which the planet was most active, after which a less dynamic period ensued that extends to the present day. The early activity left a fascinating geological record, which we are only beginning to unravel through direct observation and modeling. In considering this time period, questions outnumber answers, and one of the purposes of the meeting was to gather some of the best experts in the field to consider the current state of knowledge, ascertain which questions remain to be addressed, and identify the most promising approaches to addressing those questions. The purpose of this report is to document that discussion. Throughout the planet's first billion years, planetary-scale processes-including differentiation, hydrodynamic escape, volcanism, large impacts, erosion, and sedimentation-rapidly modified the atmosphere and crust. How did these processes operate, and what were their rates and interdependencies? The early environment was also characterized by both abundant liquid water and plentiful sources of energy, two of the most important conditions considered necessary for the origin of life. Where and when did the most habitable environments occur? Did life actually occupy them, and if so, has life persisted on Mars to the present? Our understanding of early Mars is critical to understanding how the planet we see today came to be.     

Magnetism, iron minerals, and life on Mars

A short critical review is provided on two questions linking magnetism and possible early life on Mars: (1) Did Mars have an Earth-like internal magnetic field, and, if so, during which period and was it a requisite for life? (2) Is there a connection between iron minerals in the martian regolith and life? We also discuss the possible astrobiological implications of magnetic measurements at the surface of Mars using two proposed instruments. A magnetic remanence device based on magnetic field measurements can be used to identify Noachian age rocks and lightning impacts. A contact magnetic susceptibility probe can be used to investigate weathering rinds on martian rocks and identify meteorites among the small regolith rocks. Both materials are considered possible specific niches for microorganisms and, thus, potential astrobiological targets. Experimental results on analogues are presented to support the suitability of such in situ measurements.     

A non-earthcentric approach to life detection

The ultimate goal of a comprehensive life detection strategy is never to miss life when we encounter it. To accomplish this goal, we must define life in universal, that is, non-Earthcentric, measurable terms. Next, we must understand the nature of biosignatures observed from the measured parameters of life. And finally, we must have a clear idea of the end-member states for the search--what does life, past life, or no life look like (in terms of the measured parameters) at multiple spatial and temporal scales? If we can approach these problems both in the laboratory and in the field on Earth, then we have a chance of being able to detect life elsewhere in our solar system. What are the required limits of detection at each of those scales? What spatial, spectral, and temporal resolutions are necessary to detect life? These questions are actively being investigated in our group, and in this report, we present our strategy and approach to non-Earthcentric life detection.     

The search for life on Europa: limiting environmental factors, potential habitats, and Earth analogues

The putative ocean of Europa has focused considerable attention on the potential habitats for life on Europa. By generally clement Earth standards, these Europan habitats are likely to be extreme environments. The objectives of this paper were to examine: (1) the limits for biological activity on Earth with respect to temperature, salinity, acidity, desiccation, radiation, pressure, and time; (2) potential habitats for life on Europa; and (3) Earth analogues and their limitations for Europa. Based on empirical evidence, the limits for biological activity on Earth are: (1) the temperature range is from 253 to 394 K; (2) the salinity range is a(H2O) = 0.6-1.0; (3) the desiccation range is from 60% to 100% relative humidity; (4) the acidity range is from pH 0 to 13; (5) microbes such as Deinococcus are roughly 4,000 times more resistant to ionizing radiation than humans; (6) the range for hydrostatic pressure is from 0 to 1,100 bars; and (7) the maximum time for organisms to survive in the dormant state may be as long as 250 million years. The potential habitats for life on Europa are the ice layer, the brine ocean, and the seafloor environment. The dual stresses of lethal radiation and low temperatures on or near the icy surface of Europa preclude the possibility of biological activity anywhere near the surface. Only at the base of the ice layer could one expect to find the suitable temperatures and liquid water that are necessary for life. An ice layer turnover time of 10 million years is probably rapid enough for preserving in the surface ice layers dormant life forms originating from the ocean. Model simulations demonstrate that hypothetical oceans could exist on Europa that are too cold for biological activity (T < 253 K). These simulations also demonstrate that salinities are high, which would restrict life to extreme halophiles. An acidic ocean (if present) could also potentially limit life. Pressure, per se, is unlikely to directly limit life on Europa. But indirectly, pressure plays an important role in controlling the chemical environments for life. Deep ocean basins such as the Mariana Trench are good analogues for the cold, high-pressure ocean of Europa. Many of the best terrestrial analogues for potential Europan habitats are in the Arctic and Antarctica. The six factors likely to be most important in defining the environments for life on Europa and the focus for future work are liquid water, energy, nutrients, low temperatures, salinity, and high pressures.