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Index
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 660-677
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Preface
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp xiii-xxii
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Summary
It has been almost a century since the inquiry into life's origin has been reinvigorated following several decades of quiescence influenced by Louis Pasteur's elegant experimental demonstration that microbes were not spontaneously generated in flasks of nutrient broth appropriately aerated to prevent the entry of airborne particles. It has been a century in which biochemistry and biophysics have completely altered our core understanding of the living world and consequently opened up a series of powerful experimental, theoretical, and computational approaches. In this new light, two of us independently thinking of first life were some fifteen years ago introduced by colleagues at the Santa Fe Institute who had detected some common points of interest in what we were investigating, one from the top down and the other from the bottom up – from the phenomenology of the living world with an emphasis on biochemistry and biophysics and from the underlying physics and chemistry and statistical theory that impose a necessary order.
A common theme was that life on Earth was not the outcome of an isolated event as suggested by the Chance and Necessity school but a planetary property that appeared early in the history of the planet and spread in a spontaneous way. What we designate life or proto-life has existed over most of the lifetime of planet Earth. The universality of the phenomenon and the massive flux of matter and energy due to the huge interaction of organisms and their products with the rest of planetary matter led us to return to the perceptive book Geochemistry by Kalervo Rankama and Th. G. Sahama [664], a work highly praised to one of us by the polymath G. Evelyn Hutchinson, dean of American ecologists. The two Finnish geochemists, acting as geological generalists, divided the planet into four geospheres: the lithosphere, the hydrosphere, the atmosphere, and the biosphere. The term “biosphere” had been introduced in 1875 by Eduard Suess and used in its modern sense some years later by the perceptive geochemist Vladimir Vernadsky.
What we wish to understand from a scientific point of view is how the newly formed planet, condensing approximately 4.6 billion years ago, was transformed over time into the present verdant world, home to millions of species and the abode of Homo sapiens, a taxon including individuals like ourselves, who are somehow impelled to ask the foundational questions that this work tries to answer.
3 - The geochemical context and embedding of the biosphere
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 73-169
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Summary
The chemical non-equilibrium order of life grows out of a much larger context of non-equilibrium order, occurring at scales from the formation of the Sun and planetary system, to the complex chemical environments and dynamics within the Earth's core and mantle, oceans, and atmosphere. Many disequilibria on Earth result from slow relaxation timescales in late-stage planet formation; with respect to these the Earth is still a “young” planet. These include partitioning of redox states of transition metals in the core, mantle, crust, and oceans; the slow process of partitioning of volatiles among the lithosphere, hydrosphere, and atmosphere; the escape of hydrogen and atmospheric photochemistry that move the atmosphere far from redox equilibrium with the mantle; and tectonic circulation below the crust, ocean circulation through it, and weather above it. Many of these disequilibria focus energy to an extreme degree on the rock/water interface and in the mixing chemistry of fluids and volatiles in and near the crust. Complex processes of crust formation at spreading centers drive fluid/rock interactions that both depend on and modify the chemistry of the oceans and atmosphere. Ecosystems supported by rock/water chemical disequilibria are the phylogenetically most basal and biochemically simplest, and in some ways the most conservative living systems on Earth. They have been put forth as models for the first life, and may serve as useful models if we are careful to recognize several key respects in which the Archean Earth was different from the Earth today. Here we first ask whether the same chemical stresses that support life today could have driven the emergence of the biosphere as a necessary planetary subsystem.
Order in the abiotic context for life
The order of life is inherently dynamical and dependent on forces and flows that keep living systems driven away from thermodynamic equilibrium. This fact was appreciated by Boltzmann in 1886, and has since been repeated sufficiently often [98, 570, 654, 711] to qualify as part of the common knowledge of the physics of living systems. However, to fully understand the non-equilibrium order of life it is necessary to recognize its context in a much larger field of non-equilibrium order that ranges in scope from the formation of the Sun and planetary systems, to the large-scale structure and energetics of the Earth, and down to complex webs of mechanism in planetary chemistry.
5 - Higher-level structures and the recapitulation of metabolic order
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 273-339
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Summary
Metabolism exists on Earth today only in a context formed by multiple higher-level structures, which are themselves constructed by living processes. In this chapter we consider four kinds of higher-level living order: ribosomal translation, some broad classes of oligomer catalysts, the tripartite bioenergetic system of redox couples, protons, and phosphate esters, and cellular compartmentalization including the association of cells with genomes. Like metabolism considered in Chapter 4, these higher levels show modular architecture and suggest a history of independent subsystems that were brought together to form extant cells. Many of the module boundaries follow divisions already seen in metabolism. Biosynthetic pathway patterns and a layered structure in the genetic code may reflect layers in the accretion of components of the translation system. The unification of bioenergetics by cells mirrors hierarchy in biochemistry, with a core of redox and thioester activation, and large-scale incorporation of phosphates only later, perhaps enabling the rise of an oligomer world. The cell is not merely one kind of compartment but at least three. The three core functions of cellularization – unification of bioenergetics, catalytic rate enhancement, and homeostatic regulation of the cytosol – may have come at different stages of separation from mineral-hosted environments. The resulting picture of life is of a confederacy of subsystems, which retain some distinct identity even in their current union. During biogenesis these gained autonomy from the environments that drove them into existence by becoming more dependent on each other.
Coupled subsystems and shared patterns
Universal metabolism at the ecosystem level is the chemical source of life, and (as we will argue in Chapter 8) in many respects its informatic foundation as well. However, the distinctive chemistry of living systems only occurs on Earth today in a context of elaborate higher-level structure. Biosynthesis depends in essential ways on catalysis by oligomers synthesized through ribosomal translation, on integrated and regulated bioenergetic systems, and on containment in cells. The maintenance and optimization of all these systems takes place through selection on genes and genomes, which must then be transmitted together during descent to maintain their functionality. These higher-level systems present whole webs of interdependency and entwined chicken-egg paradoxes. To understand the origin of life we cannot only pursue the relations of metabolism to geochemistry.We must also decipher the relations among these higher-level structures into patterns of serial dependency.
7 - The phase transition paradigm for emergence
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 424-538
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This chapter asks not how, but why a non-equilibrium system like the biosphere should have emerged, and how such a state can be stable. A mathematical theory exists which addresses such questions, familiar from condensed matter and particle physics as the theory of phase transitions. We show why some theory of this kind is needed to make sense of the complex facts and contradictory interpretations that have been given for the origin of life, and then introduce the fundamental concepts of phases and phase transitions in forms appropriate to the phenomena seen in earlier chapters.We introduce phase transitions as a class of mathematical phenomena, which frees us from introducing the subject by analogy, and provides a conceptually more fundamental expression of the main ideas. We show how the concepts of phase transition generalize from familiar equilibrium systems to more complex non-equilibrium cases, and summarize which lessons from equilibrium systems can be expected to generalize and where new ideas will be needed. The thermodynamic theory of stability is an application, in matter, of the method of inference known as Laplace's principle of insufficient reason, which states that when inferring from any observation, we should be as uncommittal as possible given what we have seen. From Laplace's principle, we show how the theory of optimal error correction is of the same kind as the thermal theory of stability of matter. These different versions of the stability perspective are assembled in this and the next chapter to propose that the emergence of the biosphere must be understood as a cascade of non-equilibrium phase transitions away from a lifeless Earth, and this is the origin of their necessity.
Theory in the origin of life
Many problems in reconstructing the origin of life center on searches for mechanism. We must search large parameter spaces for domains of relevance, with respect to geochemical energy sources, mineral structure and contents, organometallic and organic reactions, pathway completions, and physical structures of many kinds. The last six chapters have mostly been reviews of facts about the life we know, chosen to inform our problems of search.
A different part of understanding, alongside reconstructing the path of biogenesis, originates not in search but in conceptualization.
The Origin and Nature of Life on Earth
- The Emergence of the Fourth Geosphere
- Eric Smith, Harold J. Morowitz
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- 31 March 2016
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Uniting the conceptual foundations of the physical sciences and biology, this groundbreaking multidisciplinary book explores the origin of life as a planetary process. Combining geology, geochemistry, biochemistry, microbiology, evolution and statistical physics to create an inclusive picture of the living state, the authors develop the argument that the emergence of life was a necessary cascade of non-equilibrium phase transitions that opened new channels for chemical energy flow on Earth. This full colour and logically structured book introduces the main areas of significance and provides a well-ordered and accessible introduction to multiple literatures outside the confines of disciplinary specializations, as well as including an extensive bibliography to provide context and further reading. For researchers, professionals entering the field or specialists looking for a coherent overview, this text brings together diverse perspectives to form a unified picture of the origin of life and the ongoing organization of the biosphere.
2 - The organization of life on Earth today
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 35-72
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The biosphere that exists today is complex and heterogeneous, not only with recent, history-dependent order, but with diverse ancient forms of order that all appear to be fundamental to the nature of the living state. Rather than propose an origin of life that projects away this diversity by seeking the emergence of a single kind of entity or process, we ask what essential functions and contributions to persistence of the biosphere come from forms or order at different levels. Fundamental constraints on the possible ways to assemble living systems are captured by grouping organism phenotypes according to their chemical energy sources for electron transfers (donors or acceptors), and according to whether they are metabolically self-sufficient or can only live using resources extracted from larger ecosystems. The same bioenergetic distinctions exist for ecosystems as for organisms, but as ecosystem boundaries can often be constructed to be metabolically closed, ecosystems are in a sense simpler and more universal than organisms. The universal aspects of metabolism are ecosystem properties, and core biosynthesis powered by electron donors is more fundamental, universal, and ancient than degradative pathways that contribute much of ecological complexity. Whether the emergence of our biosphere was surprising or inevitable is not well posed as a single question; some low-level features of biochemistry seem to have inherited nearly the inevitability of geochemistry, while the character of any particular species is an epitome of chance. Key patterns, many of chemical origin, are nonetheless recapitulated across the spectrum from necessity to chance, and in some cases we can make explicit arguments that constraint flowed upward in scale from metabolic foundations because chemistry dictates paths of least resistance for evolution across a wide range of scales.
Many forms of order are fundamental in the biosphere
In attempting to understand the origin of life, we begin with what is understood about life on Earth today. Rather than seeking to project the many things known about the nature of the living state among the different sciences onto one or a few abstractions, we think it is preferable to acknowledge that life employs a wide range and diversity of organizing motifs. A theory of biogenesis must ultimately account for why so many forms exist and why they are so qualitatively diverse, and what role each plays in the function and maintenance of the biosphere. Major motifs that we wish to acknowledge include the following.
8 - Reconceptualizing the nature of the living state
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 539-607
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Here we bring together the empirical regularities from the first five chapters and the stability perspective from Chapter 7 to sketch an integrated theory of the emergence of the biosphere. Further required ideas, taken up in this chapter, include arguments for the importance of modular architecture in hierarchical complex systems, applications of the stability perspective to the problem of hierarchical control, and an explanation of the way modularity supports control by buffering errors. We interpret the subsystem decompositions reviewed in the empirical chapters as modules created by phase transitions, which made possible the emergence of hierarchical control, but dictated the architectures for which stability at the whole-system level was possible. The same basic relation – the affordance of modules that buffer errors – is the mechanism whereby low-level laws have repeatedly constrained the forms and functions of higher-level assemblies in biology. An essential element in the biosphere's emerging distinctness from abiotic Earth systems has been the emergence of individuality, a complex concept instantiated in many ways, and precondition for Darwinian evolution. For us individuality is not primitive, but is an organizational motif that emerges at intermediate stages in systems that already possess significant structure. Therefore Darwinian dynamics also is not a sufficient starting point to define the nature of life. We propose an alternative essence for the nature of life, in which the biosphere as a whole is the defining level of organization, energy transport through covalent bond chemistry is the essential function, and the complexity of the chemical substrate is an essential source of both complexity and stability.
Bringing the phase transition paradigm to life
The patterns presented in the first five chapters suggest that life grew out of geochemistry. Metabolism is the living subsystem closest to the lawfulness of geological processes. The ecosystem is the level of organization that carries the necessary and universal subnetworks within core metabolism, and that has hosted their accretion over geologic and evolutionary timescales.
In Chapter 7 we proposed that biogenesis took the form of a cascade of non-equilibrium phase transitions. Redox stresses, perhaps along with other chemical potentials (protons? phosphates?), forced electron flow through the graph of possible chemical reactions. Autocatalysis (at both network and single-molecule levels), by a hierarchy of first short and then longer loops, created sufficient positive feedback that the flow was concentrated into selective channels.
Frontmatter
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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Acknowledgments
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp xxiii-xxiv
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6 - The emergence of a biosphere from geochemistry
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 340-423
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Summary
The major divergence in approaches to biogenesis turns on the source and mechanisms of the first selectivity: whether it came from smallmolecule chemistry in a geochemical environment, or from a model of hierarchical control by macromolecules along the lines of Crick's Central Dogma. We argue that the emergence of life followed a path of least resistance along the “long arc of planetary disequilibrium,” involving the atmosphere, oceans, and dynamic mantle, described in Chapter 3. The major temporal stages followed the architectural layers of biochemistry described in Chapter 4. The first carbon fixation was mineral hosted. Feedbacks, initially via cofactors and later via oligomer catalysis, lifted core metabolism “off the rocks.” The emerging identity of the biosphere reflected the growth of autonomy as much as of chemical invention. Passage to an oligomer phase corresponding to the “RNA World” was a complex and heterogeneous transition, which transpired, and froze into place, in an already ordered organosynthetic context. We propose that cellularization occurred relatively late, and relied on functions of oligomers established in a mineral-hosted environment. The emergence of ribosomal translation originated in two parallel worlds of iron-RNA condensation-catalysis and template-directed ligation, which came together to form the first translation apparatus from mRNA to peptides. The refinement of translation fidelity, together with more precise RNA or DNA replication, ushered in the era of vertical descent along lines first appreciated by Carl Woese. Even in the era of evolution of effectively modern cells, many of the major transitions have been determined by biogeochemical reorganizations.
From universals to a path of biogenesis
In this chapter we suggest a sequence of stages in the emergence of life, based on the biological universals and the connection of life to the geochemical world, reviewed in the previous five chapters. We will propose that the hierarchy in extant life records a temporal sequence of stages, and that core biosynthetic pathways of living systems today reflect the pathways by which the same components first entered the incipient biosphere and dictated its form.
The emergence of a biosphere was an extended, and we believe a multistage and heterogeneous, sequence of transformations. In the early stages of this sequence, the processes that would become core biochemistry took shape but were not yet separate from a geochemical background.
4 - The architecture and evolution of the metabolic substrate
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 170-272
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Life at the ecosystem level is characterized by a nearly universal chart of core metabolism, comprising a few alternative paths for carbon fixation together with anabolic pathways for a standard set of small metabolites including cofactors and the three major classes of monomers (amino acids, nucleotides, and sugars). The universal chart is small, but serves as a foundation for all higher-level biochemical diversity. The patterns and functions in metabolism express a chemical logic of constraints and rules of assembly that make it in many ways a simple system, relying on surprisingly few fundamental mechanisms. The network architecture of metabolic reactions decomposes into modules and layers. Important motifs include autocatalytic loops either within or across hierarchical layers, repeated sequences of functional-group rearrangements, and distinctive and conserved dependence on certain catalysts – especially those involving metal reaction centers. By bringing together an analysis of functional dependencies, with comparative (phylogenetic) analysis where pathway variants exist, we argue that the layers and modules correspond to a historical sequence of accretions. For the known carbon fixation pathways we can propose a tree-like sequence of elaborations from an explicit root phenotype. Although the comparative analysis is carried out within the era of genomic evolution, many of the central organizing motifs originate in low-level chemistry, topology, or feedback dynamics, and would be expected to have constrained geochemical organization before the first cells. Chapter 5 will show that many motifs of apparently chemical origin in metabolism are recapitulated in higher-level systems such as the genetic code.
Metabolism between geochemistry and history
The layer of life that converts material and energy from the abiotic geospheres into the biomass that carries out all living processes is metabolism. It is both the interface layer that anchors life within planetary processes, and the first level in the synthetic hierarchy of living matter. Although metabolism has been the foundation that enables the variability of the rest of life, much of its own architecture is essentially constant across the tree of known organisms. Among the deepest core pathways, even quite detailed features such as the roles of specific molecules or reaction sequences show only modest and tightly structured variation. In this sense metabolism seems to straddle the transition from the necessity of geochemistry to the chance of cellular evolution.
Epilogue
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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- 31 March 2016, pp 608-610
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Summary
The study of the origin of life is no longer a field in its infancy. The scientific foundation we have to build from today is enormously richer than it was fifty years ago, in facts and also in concepts. The difficulties of origins research are becoming those of a maturing field with a diverse technical knowledge base: a tendency toward fragmentation and the need of more effective ways for researchers to work together as a community.
In attempting to cover this technical material, which provides the needed factual basis for generalizations and constitutes the fascinating detail about life and its planetary context, it is easy to lose sight of the profound changes in point of view that have become possible even within the past 20–30 years. We are struck by how many key points in this argument we did not understand when we were introduced to the field, but which are now fundamental to our view of the origin and nature of life.
• The universality, the historical depth, and the striking economy and conservatism of core metabolism discovered within microbiology; within that, the overarching organizing roles of the TCA cycle and one-carbon reduction.
• The greater continuity that can now be seen between chemical reactions carried out on mineral substrates, those catalyzed by small molecules, and those catalyzed by enzymes.
• The complexity of the concept of individuality and its multifarious realizations, and the complementary importance of ecosystems, culminating in the biosphere as a whole.
• The degree to which a picture can be formed of the interacting dynamics of planetary subsystems during planet formation and early evolution, and within these the role of the aggregate biosphere as a geosphere and its feedback on the other geospheres.
• A better formulation of the nature of thermodynamic limits, integrating in a seamless way the dynamical and inferential interpretations, equilibrium and disequilibrium, and stabilization and error correction.
• An appreciation of the coherence of the concepts of phase and phase transition, the way they underpin and enable reductionist science by dividing continuous scales with hierarchies of ceilings and floors, and the enormous scope of their application, beginning with a comprehensive theory of matter, and we argue, continuing that theory eventually to a theory of life.
Contents
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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References
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- 31 March 2016, pp 611-659
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1 - The planetary scope of biogenesis: the biosphere is the fourth geosphere
- Eric Smith, Tokyo Institute of Technology, Harold J. Morowitz, George Mason University, Virginia
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- The Origin and Nature of Life on Earth
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Summary
The origin of life was a planetary process, in which a departure from non-living states led to a new kind of order for matter and energy on this planet. To capture the role of life as a planetary subsystem we draw on the concept of geospheres from geology. Three traditional geospheres – the atmosphere, hydrosphere, and lithosphere – partition terrestrial matter into three physical states, each associated with a characteristic energetics and chemistry. The emergence of life brought the biosphere into existence as a fourth geosphere. The biosphere is an inherently dynamical state of order, which produces unique channels for energy flow through processes in carbon-based chemistry. The many similarities, and the interdependence, of biochemistry with organometallic chemistry of the lithosphere/hydrosphere interface, suggests a continuity of geochemistry with the earliest biochemistry. We will argue that dynamical phase transitions provide the appropriate conceptual frame to unify chance and necessity in the origin of life, and to express the lawfulness in the organization of the biosphere. The origin of life was a cascade of non-equilibrium phase transitions, and biochemistry at the ecosystem level was the bridge from geochemistry to cellular life and evolution. The universal core of metabolism provides a frame of reference that stabilizes higher levels of biotic organization, and makes possible the complexity and open-ended exploration of evolutionary dynamics.
A new way of being organized
The emergence of life on Earth brought with it, for the first time on this planet, a new way for matter and energy to be organized. Our goal is to understand this transition, how it happened and what it means. The question how life emerged – what sequence of stages actually occurred historically – can at present be answered only at the level of sketches and suggestions, though for some stages we believe good enough arguments can be made to guide experiments. To arrive at a sketch, however, we cannot escape making many choices of interpretation, of things known about life and its planetary context.
Life emerged in an era not accessible to us through historical reconstruction. Our claims about what happened in this era will depend on the principles we use to generalize, simplify, and extrapolate from knowledge of modern life and a few fossilized signatures that become increasingly fragmentary and difficult to interpret on the approach to the beginning that we wish to understand.
18 - Framing the question of fine-tuning for intermediary metabolism
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- By Eric Smith, Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, Harold J. Morowitz, Krasnow Institute for Advanced Study, East Building 207
- Edited by John D. Barrow, University of Cambridge, Simon Conway Morris, University of Cambridge, Stephen J. Freeland, University of Maryland, Baltimore, Charles L. Harper, Jr
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- Fitness of the Cosmos for Life
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- 18 December 2009
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- 06 December 2007, pp 384-420
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Learning from our own existence
Hoyle's [1] successful prediction of the 7.6 MeV resonance of the carbon-12 nucleus, based on observation of his own carbon-based existence, established the scientific usefulness of anthropic principles. These principles have become common, if not yet standard, tools in cosmology, where theories of initial conditions may not yet exist – or, if they do exist, may admit a range of values [2, 3, 4, 5, 6]. At the same time, anthropic principles have retained a traditional role in religion and philosophy, where sensitive dependence of human existence on laws of nature that could imaginably have been otherwise is interpreted as evidence for human significance in the creation of the universe.
The tendency of life forms to make universal use of, and seemingly to depend on, specific details of natural law or historical circumstance does not end with nuclear abundances. Following decades of studying the ways in which mammalian blood achieves homeostasis by exploiting favorable regions in carbonic-acid chemistry and similar adaptations, Henderson compiled a list of such dependences in physiology [7]. Inverting Darwin's description of selective fine-tuning of organisms for “fit” to their environments, Henderson characterized his physiological sensitivities anthropically as evidence of “the fitness of the environment” for life.
The rapid growth in understanding of biology, from structures to systems, seems likely to expose many more sensitivities of life to details of chemistry, physics, and history.