A robust, agnostic molecular biosignature based on machine learning.

The search for definitive biosignatures-unambiguous markers of past or present life-is a central goal of paleobiology and astrobiology. We used pyrolysis-gas chromatography coupled to mass spectrometry to analyze chemically disparate samples, including living cells, geologically processed fossil organic material, carbon-rich meteorites, and laboratory-synthesized organic compounds and mixtures. Data from each sample were employed as training and test subsets for machine-learning methods, which resulted in a model that can identify the biogenicity of both contemporary and ancient geologically processed samples with ~90% accuracy. These machine-learning methods do not rely on precise compound identification: Rather, the relational aspects of chromatographic and mass peaks provide the needed information, which underscores this method's utility for detecting alien biology.

On the roles of function and selection in evolving systems.

Physical laws-such as the laws of motion, gravity, electromagnetism, and thermodynamics-codify the general behavior of varied macroscopic natural systems across space and time. We propose that an additional, hitherto-unarticulated law is required to characterize familiar macroscopic phenomena of our complex, evolving universe. An important feature of the classical laws of physics is the conceptual equivalence of specific characteristics shared by an extensive, seemingly diverse body of natural phenomena. Identifying potential equivalencies among disparate phenomena-for example, falling apples and orbiting moons or hot objects and compressed springs-has been instrumental in advancing the scientific understanding of our world through the articulation of laws of nature. A pervasive wonder of the natural world is the evolution of varied systems, including stars, minerals, atmospheres, and life. These evolving systems appear to be conceptually equivalent in that they display three notable attributes: 1) They form from numerous components that have the potential to adopt combinatorially vast numbers of different configurations; 2) processes exist that generate numerous different configurations; and 3) configurations are preferentially selected based on function. We identify universal concepts of selection-static persistence, dynamic persistence, and novelty generation-that underpin function and drive systems to evolve through the exchange of information between the environment and the system. Accordingly, we propose a "law of increasing functional information": The functional information of a system will increase (i.e., the system will evolve) if many different configurations of the system undergo selection for one or more functions.

Abundant phosphorus expected for possible life in Enceladus's ocean.

Saturn's moon Enceladus has a potentially habitable subsurface water ocean that contains canonical building blocks of life (organic and inorganic carbon, ammonia, possibly hydrogen sulfide) and chemical energy (disequilibria for methanogenesis). However, its habitability could be strongly affected by the unknown availability of phosphorus (P). Here, we perform thermodynamic and kinetic modeling that simulates P geochemistry based on recent insights into the geochemistry of the ocean-seafloor system on Enceladus. We find that aqueous P should predominantly exist as orthophosphate (e.g., HPO42-), and total dissolved inorganic P could reach 10-7 to 10-2 mol/kg H2O, generally increasing with lower pH and higher dissolved CO2, but also depending upon dissolved ammonia and silica. Levels are much higher than <10-10 mol/kg H2O from previous estimates and close to or higher than ∼10-6 mol/kg H2O in modern Earth seawater. The high P concentration is primarily ascribed to a high (bi)carbonate concentration, which decreases the concentrations of multivalent cations via carbonate mineral formation, allowing phosphate to accumulate. Kinetic modeling of phosphate mineral dissolution suggests that geologically rapid release of P from seafloor weathering of a chondritic rocky core could supply millimoles of total dissolved P per kilogram of H2O within 105 y, much less than the likely age of Enceladus's ocean (108 to 109 y). These results provide further evidence of habitable ocean conditions and show that any oceanic life would not be inhibited by low P availability.

Historical natural kinds and mineralogy: Systematizing contingency in the context of necessity.

The advancement of science depends upon developing classification protocols that systematize natural objects and phenomena into "natural kinds"-categorizations that are conjectured to represent genuine divisions in nature by virtue of playing central roles in the articulation of successful scientific theories. In the physical sciences, theoretically powerful classification systems, such as the periodic table, are typically time independent. Similarly, the standard classification of mineral species by the International Mineralogical Association's Commission on New Minerals, Nomenclature, and Classification relies on idealized chemical composition and crystal structure, which are time-independent attributes selected on the basis of theoretical considerations from chemical theory and solid-state physics. However, when considering mineral kinds in the historical context of planetary evolution, a different, time-dependent classification scheme is warranted. We propose an "evolutionary" system of mineral classification based on recognition of the role played by minerals in the origin and development of planetary systems. Lacking a comprehensive theory of chemical evolution capable of explaining the time-dependent pattern of chemical complexification exhibited by our universe, we recommend a bootstrapping approach to mineral classification based on observations of geological field studies, astronomical observations, laboratory experiments, and analyses of natural samples and their environments. This approach holds the potential to elucidate underlying universal principles of cosmic chemical complexification.

An evolutionary system of mineralogy. Part III: Primary chondrule mineralogy (4566 to 4561 Ma).

Information-rich attributes of minerals reveal their physical, chemical, and biological modes of origin in the context of planetary evolution, and thus they provide the basis for an evolutionary system of mineralogy. Part III of this system considers the formation of 43 different primary crystalline and amorphous phases in chondrules, which are diverse igneous droplets that formed in environments with high dust/gas ratios during an interval of planetesimal accretion and differentiation between 4566 and 4561 Ma. Chondrule mineralogy is complex, with several generations of initial droplet formation via various proposed heating mechanisms, followed in many instances by multiple episodes of reheating and partial melting. Primary chondrule mineralogy thus reflects a dynamic stage of mineral evolution, when the diversity and distribution of natural condensed solids expanded significantly.

Quantifying ecological impacts of mass extinctions with network analysis of fossil communities.

Mass extinctions documented by the fossil record provide critical benchmarks for assessing changes through time in biodiversity and ecology. Efforts to compare biotic crises of the past and present, however, encounter difficulty because taxonomic and ecological changes are decoupled, and although various metrics exist for describing taxonomic turnover, no methods have yet been proposed to quantify the ecological impacts of extinction events. To address this issue, we apply a network-based approach to exploring the evolution of marine animal communities over the Phanerozoic Eon. Network analysis of fossil co-occurrence data enables us to identify nonrandom associations of interrelated paleocommunities. These associations, or evolutionary paleocommunities, dominated total diversity during successive intervals of relative community stasis. Community turnover occurred largely during mass extinctions and radiations, when ecological reorganization resulted in the decline of one association and the rise of another. Altogether, we identify five evolutionary paleocommunities at the generic and familial levels in addition to three ordinal associations that correspond to Sepkoski's Cambrian, Paleozoic, and Modern evolutionary faunas. In this context, we quantify magnitudes of ecological change by measuring shifts in the representation of evolutionary paleocommunities over geologic time. Our work shows that the Great Ordovician Biodiversification Event had the largest effect on ecology, followed in descending order by the Permian-Triassic, Cretaceous-Paleogene, Devonian, and Triassic-Jurassic mass extinctions. Despite its taxonomic severity, the Ordovician extinction did not strongly affect co-occurrences of taxa, affirming its limited ecological impact. Network paleoecology offers promising approaches to exploring ecological consequences of extinctions and radiations.

An evolutionary system of mineralogy. Part I: Stellar mineralogy (>13 to 4.6 Ga).

Minerals preserve records of the physical, chemical, and biological histories of their origins and subsequent alteration, and thus provide a vivid narrative of the evolution of Earth and other worlds through billions of years of cosmic history. Mineral properties, including trace and minor elements, ratios of isotopes, solid and fluid inclusions, external morphologies, and other idiosyncratic attributes, represent information that points to specific modes of formation and subsequent environmental histories-information essential to understanding the co-evolving geosphere and biosphere. This perspective suggests an opportunity to amplify the existing system of mineral classification, by which minerals are defined solely on idealized end-member chemical compositions and crystal structures. Here we present the first in a series of contributions to explore a complementary evolutionary system of mineralogy-a classification scheme that links mineral species to their paragenetic modes. The earliest stage of mineral evolution commenced with the appearance of the first crystals in the universe at >13 Ga and continues today in the expanding, cooling atmospheres of countless evolved stars, which host the high-temperature (T > 1000 K), low-pressure (P < 10-2 atm) condensation of refractory minerals and amorphous phases. Most stardust is thought to originate in three distinct processes in carbon- and/or oxygen-rich mineral-forming stars: (1) condensation in the cooling, expanding atmospheres of asymptotic giant branch stars; (2) during the catastrophic explosions of supernovae, most commonly core collapse (Type II) supernovae; and (3) classical novae explosions, the consequence of runaway fusion reactions at the surface of a binary white dwarf star. Each stellar environment imparts distinctive isotopic and trace element signatures to the micro- and nanoscale stardust grains that are recovered from meteorites and micrometeorites collected on Earth's surface, by atmospheric sampling, and from asteroids and comets. Although our understanding of the diverse mineral-forming environments of stars is as yet incomplete, we present a preliminary catalog of 41 distinct natural kinds of stellar minerals, representing 22 official International Mineralogical Association (IMA) mineral species, as well as 2 as yet unapproved crystalline phases and 3 kinds of non-crystalline condensed phases not codified by the IMA.

An evolutionary system of mineralogy. Part II: Interstellar and solar nebula primary condensation mineralogy (>4.565 Ga).

The evolutionary system of mineralogy relies on varied physical and chemical attributes, including trace elements, isotopes, solid and fluid inclusions, and other information-rich characteristics, to understand processes of mineral formation and to place natural condensed phases in the deep-time context of planetary evolution. Part I of this system reviewed the earliest refractory phases that condense at T > 1000 K within the turbulent expanding and cooling atmospheres of highly evolved stars. Part II considers the subsequent formation of primary crystalline and amorphous phases by condensation in three distinct mineral-forming environments, each of which increased mineralogical diversity and distribution prior to the accretion of planetesimals >4.5 billion years ago. INTERSTELLAR MOLECULAR SOLIDS: (1)Varied crystalline and amorphous molecular solids containing primarily H, C, O, and N are observed to condense in cold, dense molecular clouds in the interstellar medium (10 < T < 20 K; P < 10-13 atm). With the possible exception of some nanoscale organic condensates preserved in carbonaceous meteorites, the existence of these phases is documented primarily by telescopic observations of absorption and emission spectra of interstellar molecules in radio, microwave, or infrared wavelengths. NEBULAR AND CIRCUMSTELLAR ICE: (2)Evidence from infrared observations and laboratory experiments suggest that cubic H2O ("cubic ice") condenses as thin crystalline mantles on oxide and silicate dust grains in cool, distant nebular and circumstellar regions where T ~100 K. PRIMARY CONDENSED PHASES OF THE INNER SOLAR NEBULA: (3)The earliest phase of nebular mineralogy saw the formation of primary refractory minerals that solidified through high-temperature condensation (1100 < T < 1800 K; 10-6 < P < 10-2 atm) in the solar nebula more than 4.565 billion years ago. These earliest mineral phases originating in our solar system formed prior to the accretion of planetesimals and are preserved in calcium-aluminum-rich inclusions, ultra-refractory inclusions, and amoeboid olivine aggregates.

Chance, necessity and the origins of life: a physical sciences perspective.

Earth's 4.5-billion-year history has witnessed a complex sequence of high-probability chemical and physical processes, as well as 'frozen accidents'. Most models of life's origins similarly invoke a sequence of chemical reactions and molecular self-assemblies in which both necessity and chance play important roles. Recent research adds two important insights into this discussion. First, in the context of chemical reactions, chance versus necessity is an inherently false dichotomy-a range of probabilities exists for many natural events. Second, given the combinatorial richness of early Earth's chemical and physical environments, events in molecular evolution that are unlikely at limited laboratory scales of space and time may, nevertheless, be inevitable on an Earth-like planet at time scales of a billion years.This article is part of the themed issue 'Reconceptualizing the origins of life'.

Attachment of ribonucleotides on α-alumina as a function of pH, ionic strength, and surface loading.

The interactions between nucleic acids and mineral surfaces have been the focus of many studies in environmental sciences, in biomedicine, as well as in origin of life studies for the prebiotic formation of biopolymers. However, few studies have focused on a wide range of environmental conditions and the likely modes of attachment. Here we investigated the adsorption of ribonucleotides onto α-alumina surfaces over a wide range of pH, ionic strength, and ligand-to-solid ratio, by both an experimental and a theoretical approach. The adsorption of ribonucleotides is strongly affected by pH, with a maximum adsorption at pH values around 5. Alumina adsorbs high amounts of nucleotides >2 µmol/m(2). We used the extended triple-layer model (ETLM) to predict the speciation of the surface complexes formed as well as the stoichiometry and equilibrium constants. We propose the formation of two surface species: a monodentate inner-sphere complex, dominant at pH <7, and a bidentate outer-sphere complex, dominant at higher pH. Both complexes would involve interactions between the negatively charged phosphate group and the positively charged surface of alumina. Our results provide a better understanding of how nucleic acids attach to mineral surfaces under varying environmental conditions. Moreover, the predicted configuration of nucleotide surface species, bound via the phosphate group, could have implications for the abiotic formation of nucleic acids in the context of the origin of life.

Cooperative and competitive adsorption of amino acids with Ca²âº on rutile (α-TiO2).

The interactions of biomolecules such as amino acids with mineral surfaces in the near-surface environment are an important part of the short and long-term carbon cycles. Amino acid-mineral surface interactions also play an important role in biomineralization, biomedicine, and in assembling the building blocks of life in the prebiotic era. Although the pH effects during adsorption of amino acids onto mineral surfaces have been studied, little is known about the effects of environmentally important divalent cations. In this study, we investigated the adsorption of the oppositely charged amino acids glutamate and lysine with and without the addition of divalent calcium. Without calcium, glutamate shows a maximum in adsorption at a pH of ∼4 and lysine shows a maximum in adsorption at a pH of ∼9.4. In comparison, with calcium present, glutamate showed maxima in adsorption at both low and high pH, whereas lysine showed no adsorption at all. These dramatic effects can be described as cooperative adsorption between glutamate and Ca(2+) and as competitive adsorption between lysine and Ca(2+). The origin of these effects can be attributed to electrostatic phenomena. Adsorption of Ca(2+) at high pH makes the rutile surface more positive, which attracts glutamate and repels lysine. Our results indicate that the interactions of biomolecules with mineral surfaces in the environment will be strongly affected by the major dissolved species in natural waters.

Open-ended versus bounded evolution: Mineral evolution as a case study.

To what extent are naturally evolving systems limited in their potential diversity (i.e. "bounded") versus unrestricted ("open-ended")? Minerals provide a quantitative model evolving system, with well-documented increases in mineral diversity through multiple stages of planetary evolution over billions of years. A recent framework that unifies behaviors of both biotic and abiotic evolving systems posits that all such systems are characterized by combinatorial richness subject to selection. In the case of minerals, combinatorial richness derives from the possible combinations of chemical elements coupled with permutations of their formulas' coefficients. Observed mineral species, which are selected for persistence through deep time, represent a miniscule fraction of all possible element configurations. Furthermore, this model predicts that as planetary systems evolve, stable minerals become an ever-smaller fraction of the "possibility space." A postulate is that "functional information," defined as the negative log2 of that fraction, must increase as a system evolves. We have tested this hypothesis for minerals by estimating the fraction of all possible chemical formulas observed from one stage of mineral evolution to the next, based on numbers of different essential elements and the maximum chemical formula complexity at each of nine chronological stages of mineral evolution. We find a monotonic increase in mineral functional information through these nine stages-a result consistent with the hypothesis. Furthermore, analysis of the chemical formulas of minerals demonstrates that the modern Earth may be approaching the maximum limit of functional information for natural mineral systems-a result demonstrating that mineral evolution is not open-ended.

Molecular assembly indices of mineral heteropolyanions: some abiotic molecules are as complex as large biomolecules.

Molecular assembly indices, which measure the number of unique sequential steps theoretically required to construct a three-dimensional molecule from its constituent atomic bonds, have been proposed as potential biosignatures. A central hypothesis of assembly theory is that any molecule with an assembly index ≥15 found in significant local concentrations represents an unambiguous sign of life. We show that abiotic molecule-like heteropolyanions, which assemble in aqueous solution as precursors to some mineral crystals, range in molecular assembly indices from 2 for H2CO3 or Si(OH)4 groups to as large as 21 for the most complex known molecule-like subunits in the rare minerals ewingite and ilmajokite. Therefore, values of molecular assembly indices ≥15 do not represent unambiguous biosignatures.

Atomic-scale surface roughness of rutile and implications for organic molecule adsorption.

Crystal surfaces provide physical interfaces between the geosphere and biosphere. It follows that the arrangement of atoms at the surfaces of crystals profoundly influences biological components at many levels, from cells through biopolymers to single organic molecules. Many studies have focused on the crystal-molecule interface in water using large, flat single crystals. However, little is known about atomic-scale surface structures of the nanometer- to micrometer-sized crystals of simple metal oxides typically used in batch adsorption experiments under conditions relevant to biogeochemistry and the origins of life. Here, we present atomic-resolution microscopy data with unprecedented detail of the circumferences of nanosized rutile (α-TiO2) crystals previously used in studies of the adsorption of protons, cations, and amino acids. The data suggest that one-third of the {110} faces, the largest faces on individual crystals, consist of steps at the atomic scale. The steps have the orientation to provide undercoordinated Ti atoms of the type and abundance for adsorption of amino acids as inferred from previous surface complexation modeling of batch adsorption data. A remarkably uniform pattern of step proportions emerges: the step proportions are independent of surface roughness and reflect their relative surface energies. Consequently, the external morphology of rutile nanometer- to micrometer-sized crystals imaged at the coarse scale of scanning electron microscope images is not an accurate indicator of the atomic smoothness or of the proportions of the steps present. Overall, our data strongly suggest that amino acids attach at these steps on the {110} surfaces of rutile.

Mineral-organic interfacial processes: potential roles in the origins of life.

Life is believed to have originated on Earth ∼4.4-3.5 Ga ago, via processes in which organic compounds supplied by the environment self-organized, in some geochemical environmental niches, into systems capable of replication with hereditary mutation. This process is generally supposed to have occurred in an aqueous environment and, likely, in the presence of minerals. Mineral surfaces present rich opportunities for heterogeneous catalysis and concentration which may have significantly altered and directed the process of prebiotic organic complexification leading to life. We review here general concepts in prebiotic mineral-organic interfacial processes, as well as recent advances in the study of mineral surface-organic interactions of potential relevance to understanding the origin of life.

Predicting new mineral occurrences and planetary analog environments via mineral association analysis.

The locations of minerals and mineral-forming environments, despite being of great scientific importance and economic interest, are often difficult to predict due to the complex nature of natural systems. In this work, we embrace the complexity and inherent "messiness" of our planet's intertwined geological, chemical, and biological systems by employing machine learning to characterize patterns embedded in the multidimensionality of mineral occurrence and associations. These patterns are a product of, and therefore offer insight into, the Earth's dynamic evolutionary history. Mineral association analysis quantifies high-dimensional multicorrelations in mineral localities across the globe, enabling the identification of previously unknown mineral occurrences, as well as mineral assemblages and their associated paragenetic modes. In this study, we have predicted (i) the previously unknown mineral inventory of the Mars analogue site, Tecopa Basin, (ii) new locations of uranium minerals, particularly those important to understanding the oxidation-hydration history of uraninite, (iii) new deposits of critical minerals, specifically rare earth element (REE)- and Li-bearing phases, and (iv) changes in mineralization and mineral associations through deep time, including a discussion of possible biases in mineralogical data and sampling; furthermore, we have (v) tested and confirmed several of these mineral occurrence predictions in nature, thereby providing ground truth of the predictive method. Mineral association analysis is a predictive method that will enhance our understanding of mineralization and mineralizing environments on Earth, across our solar system, and through deep time.

Evolution of the crustal phosphorus reservoir.

The release of phosphorus (P) from crustal rocks during weathering plays a key role in determining the size of Earth's biosphere, yet the concentration of P in crustal rocks over time remains controversial. Here, we combine spatial, temporal, and chemical measurements of preserved rocks to reconstruct the lithological and chemical evolution of Earth's continental crust. We identify a threefold increase in average crustal P concentrations across the Neoproterozoic-Phanerozoic boundary (600 to 400 million years), showing that preferential biomass burial on shelves acted to progressively concentrate P within continental crust. Rapid compositional change was made possible by massive removal of ancient P-poor rock and deposition of young P-rich sediment during an episode of enhanced global erosion. Subsequent weathering of newly P-rich crust led to increased riverine P fluxes to the ocean. Our results suggest that global erosion coupled to sedimentary P-enrichment forged a markedly nutrient-rich crust at the dawn of the Phanerozoic.

Speciation of L-DOPA on nanorutile as a function of pH and surface coverage using surface-enhanced Raman spectroscopy (SERS).

The adsorption configuration of organic molecules on mineral surfaces is of great interest because it can provide fundamental information for both engineered and natural systems. Here we have conducted surface-enhanced Raman spectroscopy (SERS) measurements to probe the attachment configurations of DOPA on nanorutile particles under different pH and surface coverage conditions. The Raman signal enhancement arises when a charge transfer (CT) complex forms between the nanoparticles and adsorbed DOPA. This Raman signal is exclusively from the surface-bound complexes with great sensitivity to the binding and orientation of the DOPA attached to the TiO(2) surface. Our SERS spectra show peaks that progressively change with pH and surface coverage, indicating changing surface speciation. At low pH and surface coverage, DOPA adsorbs on the surface lying down, with probably three points of attachment, whereas at higher pH and surface coverage DOPA stands up on the surface as a species involving two attachment points via the two phenolic oxygens. Our results demonstrate experimentally the varying proportions of the two surface species as a function of environmental conditions consistent with published surface complexation modeling. This observation opens up the possibility to manipulate organic molecule attachment in engineered systems such as biodetection devices. Furthermore, it provides a perspective on the possible role of mineral surfaces in the chemical evolution of biomolecules on the early Earth. Adsorbed biomolecules on mineral surface in certain configurations may have had an advantage for subsequent condensation reactions, facilitating the formation of peptides.

Evidence for the oxidation of Earth's crust from the evolution of manganese minerals.

Analysis of manganese mineral occurrences and valence states demonstrate oxidation of Earth's crust through time. Changes in crustal redox state are critical to Earth's evolution, but few methods exist for evaluating spatially averaged crustal redox state through time. Manganese (Mn) is a redox-sensitive metal whose variable oxidation states and abundance in crustal minerals make it a useful tracer of crustal oxidation. We find that the average oxidation state of crustal Mn occurrences has risen in the last 1 billion years in response to atmospheric oxygenation following a 66 ± 1 million-year time lag. We interpret this lag as the average time necessary to equilibrate the shallow crust to atmospheric oxygen fugacity. This study employs large mineralogical databases to evaluate geochemical conditions through Earth's history, and we propose that this and other mineral data sets form an important class of proxies that constrain the evolving redox state of various Earth reservoirs.