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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research 4 What Role Does Life Play in the Metabolism of Planet Earth? For the first 3 billion years of Earth’s history, all life was confined to the ocean and was entirely microbial. That life was electric. The earliest forms of life evolved a set of mechanisms for extracting energy from the chemicals around them and from sunlight by transferring electrons from one element or molecule to another. All life on Earth continues to rely on this ability to move electrons, and the electron transfer reactions, invented by the earliest bacteria and passed on to all other living organisms, form a nested set of biologically catalyzed elemental cycles. The elemental cycles are coupled to geochemical and geophysical processes that, in concert, have sustained life on Earth from the start of the geological record about 3.8 billion years ago. The biological conversion of solar energy into chemical energy ultimately became the primary source of energy for all life on the Earth’s surface. Through an obscure series of evolutionary occurrences, the highest energy state that evolved produced oxygen as a byproduct of splitting water; the hydrogen atoms were used to form organic matter from carbon dioxide. The energy in this “primary” organic matter is used by other organisms for energy and growth. Furthermore, the resulting accumulation of oxygen in Earth’s atmosphere created a large chemical energy potential, which ultimately allowed organisms to extract energy from organic matter approximately 18 times more efficiently than without oxygen. Without primitive life, Earth’s atmosphere would not have contained enough oxygen to support its current life forms, including humans. The main waste products of this oxygen-based respiratory metabolism are water and carbon dioxide. Through a series of symbiotic events, two basic and interdependent metabolic pathways—oxygenic photosynthesis and aerobic respiration—form
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research the basis of all complex multicellular life on Earth. Their evolutionary histories, inferred from gene sequences, are part of the profound record of all life forms having evolved from a few common ancestors. Metabolism is a universal feature of living systems. All organisms must acquire and transform energy into forms that they can use to make new cells and repair old ones. In the process, all organisms exchange gases with their environment. Gas exchange provides a mechanism to analyze metabolic pathways and fluxes on local and global scales. It is a crucial link between organisms and their environment. When organisms take up energy and resources and expel metabolic byproducts, they shape not only their local environment but ultimately the planetary environment (Frausto da Silva and Williams, 1996; Sterner and Elser, 2002). Although the environmental consequences of an individual organism’s metabolism can be small and localized, the metabolic effects of large collections of organisms are global. The planet is habitable for large, multicellular, air-breathing animals like humans only because other creatures have made it habitable. The atmosphere also dissipates heat and buffers temperature, which allows for relatively stable forms of life. Because the metabolisms of organisms are linked, to each other and to the atmosphere and climate, this is an area with potential for theoretical unification. There are conserved metabolic pathways by which organisms capture, transform, and dissipate energy. This chapter considers the evolution of these pathways and the interaction of energy metabolism with pivotal materials such as carbon and nitrogen. An expansive view of metabolism is taken throughout the chapter. It is considered both at the level of cells and organisms and at the level of ecological systems and the entire biosphere. This multiscale approach is essential given that it is the combined effect of individual organisms’ metabolisms, which have the potential to affect regional and global environmental conditions. An important challenge at the intersection of biology, geochemistry, and physics is to understand how the global metabolic network evolved, what the feedbacks were that led to the constrained variations in gas composition of the planetary atmosphere, and the limitations of these processes on organismal, ecological, and geological spatial and time scales. Understanding this vast global metabolic network requires developing a global “systems geobiology,” the root of which lies in the origins of life on Earth and which is deeply grounded in the fundamental physiological pathways of life. “Systems geobiology,” in this report, is defined as the integrated study incorporating geochemistry, geophysics, and other environmental sciences with genomics, ecophysiology, and mathematics to understand the processes and feedback mechanisms influencing Earth’s overall metabolism. The further goal is to improve our ability to predict responses of the Earth’s systems to external and internal perturbations. This discipline is as new as
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research it is urgently needed and will require significant theoretical investment to tie together its diverse components. The collective metabolism of human societies, which includes a variety of industrial processes in addition to human biological functions, generates enormous amounts of byproducts. Human activities have altered the composition of gases in Earth’s atmosphere, the distribution of water in terrestrial ecosystems, and nutrient regimes in rivers and along continental margins worldwide. These byproducts have consequences for the natural environments that sustain humans and also influence biospheric metabolic processes by modifying the physical environment. Knowledge of the intricacies of metabolism is critical to (1) understand the consequences of our metabolism at all scales, (2) devise and facilitate remediation strategies for the ecosystems that are degraded but crucial to sustaining humans, and (3) reduce the generation of noxious metabolic byproducts and accelerate their safe disposal. The issues addressed by systems geobiology are fundamental in public discourse; these issues include understanding the importance of metabolism for all life on Earth and the extent to which specific metabolic processes can be altered to ameliorate human-caused effects on biogeochemical cycles. Systems geobiology cuts across traditional disciplinary boundaries. For example, global metabolic fluxes are the cumulative result of the specific capabilities of individual molecules, powering individual cells in different organisms, which themselves interact in many different communities. Research in this area requires expertise in microbiology, enzymology, protein chemistry, cell biology, biophysics, comparative physiology, geochemistry, and ecology, among others. These topics therefore require the combined skills of physical scientists and biologists of all kinds. Practitioners of this new science have to work at many scales that span from genomics to the atmospheric sciences. The broadly integrative training approach of the physiological sciences will likely be invaluable in training students of the Earth’s “physiology.” Such an interdisciplinary approach is rare in biological curricula. One possible course curriculum would begin with an overview of the metabolic processes of archaea and bacterial cells, outline the evolution of these processes during Earth’s history, and conclude with an overview of the biosphere’s biogeochemical cycles. THE ROOTS OF METABOLISM The ability to acquire energy and convert it to biologically usable forms (energy transduction) depends on a few, virtually immutable, complex molecular machines. These machines catalyze reactions in which electrons are transferred from reduced, high-energy molecules to a small set of molecules that act as energy transfer receptacles. All known energy transduction
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research machines evolved in microorganisms over 2.5 billion years ago and were spread across all domains of life by lateral gene transfer and endosymbiotic events. The relatively free exchange of metabolic machines early in the history of life has resulted in a set of core metabolic pathways shared by all organisms. Although biologists do not have a detailed understanding of how these energy transfer machines evolved on a subcellular level, these shared molecular entities now form an interdependent planetary “electron market” where reductants and oxidants are exchanged across the globe. The scale of this electron market is planetary because gases, produced by all organisms, can be transported around Earth’s surface by the ocean and the atmosphere. From a metabolic perspective, living systems use a relatively small suite of conserved ancient pathways. The vast diversity of metabolic pathways can be divided into sets of metabolic circuits that perform three different functions (Figure 4-1). The first set of circuits is devoted to acquiring environmental energy. Living systems harvest energy from sunlight and from inorganic and organic compounds, and they transfer this energy to electron or hydrogen carriers. The second set of circuits uses the energy of oxidation or reduction (redox) reactions to pump ions across membranes to establish ionic charge gradients. Once an electron is accepted, it flows downhill (in an energy sense) until the circuit is closed by the reduction of an electron acceptor. The charged membrane is a biological capacitor that serves several different functions, among the most significant of which is the synthesis of adenosine triphosphate (ATP), the universal high-energy compound of living systems. A third circuit of reactions serves to employ a source of carbon and energy-rich molecules to synthesize new organic compounds, and thus make new cells and repair old ones. All the anabolic reactions required to manufacture cells and the tissues of multicellular organisms are in this category. The previous chapter discussed the diversity of life forms and functions that evolution has generated. By contrast, the universality of the genes, proteins, and compounds that participate in these three sets of metabolic pathways is noteworthy (Benner et al., 2002). The molecules that transport energy used by various living systems are, for the most part, the same and seem to be a near-universal feature of life on this planet. Organisms ranging from anaerobic archaea and bacteria to strictly aerobic animals have adopted nicotine adenine dinucleotide (NAD), flavins, and quinones as their energy carriers. Genomic data show that the pathways used to synthesize these compounds can be found across the boundaries of life’s domains. The reactions for energy transduction are found in archaea and bacteria and are present in eukaryotes as well, as a result of an ancient endosymbiosis (Nealson and Rye, 2005). The enzymes responsible for the hydrolysis of ATP and the genes that code for them are abundant in most organisms. Those
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research FIGURE 4-1 The three fundamental energy metabolism processes: (1) The formation of reduced products from sunlight, organic molecules, or inorganic reduced molecules. Energy is transferred to reduced hydrogen or electron carriers that are then used directly for anabolic reactions (3), for C or N fixation, or for (2) the generation of adenosine triphosphate (ATP). ATP is generated by the pumping of cations (usually protons, H+) across a semipermeable membrane to establish a gradient. Many anabolic functions (3) require ATP and/or reducing equivalents. SOURCE: Reprinted from Treatise on Geochemistry: Volume 8, Biogeochemistry, K. H. Nealson and R. Rye, Evolution of Metabolism, Pages 41-61, Copyright 2005, with permission from Elsevier. enzymes and genes have been co-opted to perform all sorts of other functions, many of which now have nothing to do with ATP (Saier, 2000). All three domains of life appear to use similar approaches for energy capture and transduction and the same (or very similar) molecules to fulfill these two functions. Either the last common ancestor of the three domains had already evolved these processes or these processes were widely exchanged by lateral transfer, and the now common processes proved to be
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research better than their alternatives. In either case, it is likely that the evolution of life’s redox chemistry (and the diversity of pathways that it now has) evolved very early in the history of life, long before the deposition of the first macrofossils. There is a global integration of the planet’s metabolism. The composition of the atmosphere, and hence the conditions for life, is the result of the balance of inorganic processes and of complementary metabolic processes. The biogeochemical tension between nitrification and denitrification and photosynthesis are good examples. The metabolism of living systems and the physical state of the planet are linked by complex and still poorly understood feedbacks. An important challenge for the future of the biological sciences is to forge collaborations with the geosciences with the goal of understanding the full metabolic network of the planet. METABOLISM: A CELLULAR PROCESS WITH GLOBAL CONSEQUENCES The study of metabolic processes, in all their guises, is a unifying theme in biology. Studying metabolism, the flow of energy and molecules in the cell, at almost any level of organization is a challenging enterprise that demands the development of imaginative conceptual approaches and new technologies (Box 4-1). One of the promises of systems biology (including the integration of transcriptomics, proteonomics, and metabolomics) is to develop adequate working models of metabolic cell function. Establishing the link between macromolecular structure and metabolic function is also a goal of many disciplines in biology, ranging from organismal physiology to ecosystem and planetary ecology. Indeed, the interdisciplinary approach that organismal biologists use to investigate the function of whole organisms might be the best model for how to teach, study, and communicate metabolism to the public (Feder, 2005). At the higher levels of organization, the conceptual and technological challenges are as difficult as they are urgent. Humans are exerting a major impact on the metabolic fluxes of the planet. An understanding of biosphere-atmosphere interactions requires integrated input from biology, atmospheric science, and geology. The role and importance of the physiological processes of plants, microorganisms, and animals in both terrestrial and marine environments on the composition and behavior of the atmosphere still need to be fully characterized. The processes that shape biosphere-atmosphere interactions occur at many spatial scales and can take place over decades and centuries. New actors in this system continue to be discovered, like the archaea that are major consumers of methane in oxygen-free sediments (Raghoebarsing et al., 2006).
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research BOX 4-1 Stable Isotopes Reveal the Global Influence of Metabolism The observation of enzyme-driven molecular effects at the planetary level reveals the immensity of the magnitude of life’s metabolism. Remarkably, these global-scale signals can be re-created in test tubes and in greenhouses. Just as researchers interested in systems biology and in tracking the evolution of biological systems rely on nucleic acids and the polymerase chain reaction (PCR), ecologists interested in measuring the fluxes of energy and materials among components of ecological systems (ranging from cells to the whole biosphere) increasingly rely on stable isotope analyses. Interpreting the stable isotope signals of life’s metabolism requires putting together information derived from the study of metabolic processes at levels that range from cells to broad geographical regions. All the macromolecules that comprise life are composed of six major elements: H, C, N, O, S, and P. Of those the first five have stable isotopes that can be distinguished by their mass. The enzymes that mediate metabolic reactions are often sensitive to differences in the dissociation energies of molecules with different isotopes in them. Consequently, molecules that contain isotopes of different masses are incorporated differentially into the products of incomplete metabolic reactions. For example, in oxygenic autotrophs (organisms that use the energy from sunlight to produce sugars, releasing oxygen as a byproduct), Rubisco (ribulose 1,5-biphosphate carboxylase-oxygenase) fixes CO2 to make sugars. This enzyme discriminates against CO2 containing 13C and produces sugars that are greatly depleted in this isotope. Because Rubisco is the most abundant enzyme on Earth and processes enormous amounts of CO2, there is a substantial accumulation of 13C in organic matter buried in the lithosphere and in the isotopic composition of the atmosphere. On land the fixation of CO2 varies seasonally and seasonal changes in 13C concentration can be observed in atmospheric air. CO2 dissolves in the ocean with little discrimination. Therefore, 13C is useful to distinguish CO2 uptake by terrestrial vegetation and by dissolution in the oceans. Similarly, during respiration, 16O (i.e., O2 containing two atoms of 16O) is preferentially used to oxidize organic matter, leaving the major heavier isotope 18O in the atmosphere. In contrast, there is virtually no fractionation of oxygen isotopes in photosynthesis. Hence, variations in the 18O/16O ratio provide a geochemical framework to assess how closely coupled photosynthesis and respiration are on geological time scales (Sowers and Bender, 1995). The geological records of S and N isotopes reflect the oxidation state of the oceans and atmosphere, as well as periods when the Earth’s systems were greatly perturbed (e.g., through mass extinction events). Understanding how the Earth systems responded to these perturbations and the time scale of recovery is critically important, as human perturbations potentially can force the planetary atmosphere/climate into a new mode, very different from that which humans have experienced since the evolution of Homo sapiens ~ 200,000 years ago. This understanding requires an integration of knowledge from the physical bases of isotopic fractionation to the molecular processes responsible for the observed isotopic variations. Biologists will need to be trained so that they are capable of adopting new tools like this that cut across levels of organization and that allow scaling up the consequences of the molecular details of metabolic enzyme function to their global effects.
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research The study of biosphere-atmosphere interactions, therefore, emphasizes the use of model simulations (Moorcroft, 2006). Nonetheless, these models need to be informed by laboratory experiments that probe the responses of organisms to changes in the atmosphere and by reliable measurements of the relevant gas fluxes. These require sophisticated gas exchange methodologies and remote sensing techniques to scale up what are now, by necessity, sporadic measurements with respect to relevant geographical scales. So far, coupled biosphere-atmosphere models have largely avoided accounting for the diversity of function in the organisms that make up real ecosystems. It is clear that biosphere-atmosphere models cannot yet account for all the details and all the biological structure in ecosystems. However, it might be possible to group organisms into functional groups based on the effect of diversity in physiology with respect to the atmosphere. Indeed, ecologists have now begun to measure variation in the function of microorganisms and plants at the global scales that are appropriate to account for biosphere-atmosphere interactions. Life’s metabolism is changing and continues to change and shape the atmosphere. But the atmosphere has also shaped life. To go beyond this simple observation, it is necessary to create a predictive science of the biosphere’s metabolism and its effect on the atmosphere. This now stands as a major challenge for biology, helping to advance the science of the Earth’s metabolism. The metabolism inside a cell has profound consequences for the environment in which that cell exists. For example, large-scale heat production is critical for complex behavior in metazoans and is the base for endothermy in mammals and birds. Large-scale heat production also occurs in microbial communities, in termite and ant colonies, and at ecosystem levels, when forests and phytoplankton dissipate large fractions of absorbed solar energy, thereby altering the thermal structure of the local environment (Lewis et al., 1990; Gates, 2003). One mechanism involved in generating heat involves the two primary products of energy transformation: ATP and nicotinamide adenine dinucleotide phosphate (NAD [P]). The former is required for catalysis, macromolecular synthesis, and protein conformation. The latter is required for redox reactions. How ATP/NAD(P)H ratios are controlled at the cellular level is still poorly understood, but the ratio of these two molecules is critical in determining energy transformation efficiency. Excess production of ATP can be coupled to exergonic reactions, thereby dissipating energy as heat. Photosynthesis appears to have evolved in the early Archean (>3 billion years ago), although exactly when remains unclear. Initially, the process was almost certainly anaerobic; the energy of the sun was used to extract electrons and/or protons from relatively low energy molecules and elements including hydrogen sulfide (H2S), ferrous iron (FeII), and even preformed organic matter (CH2O) to chemically reduce CO2 to form organic mat-
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research ter. By the late Archean and early Proterozoic (approximately 2.5 billion years ago), geochemical data suggest that water (H2O; a reduced form of oxygen) was oxidized by photosynthetic organisms to produce molecular oxygen (O2). The burial of the photosynthetically produced organic matter in ocean sediments allowed oxygen to accumulate in Earth’s atmosphere. Indeed, without the burial of organic matter—a geologically controlled process—Earth would have remained anaerobic. The slow rise of oxygen through the mid to late Proterozoic altered forever the metabolic networks that subsequently evolved in the first half of Earth’s history. Oxygen is an extremely strong oxidant; when coupled to the oxidation of organic matter, it yields up to 18 times more energy than anaerobic metabolism. The evolution of oxygen in Earth’s atmosphere and oceans “supercharged” biological metabolism, ultimately facilitating much faster metabolic fluxes of elements through biological systems. The use of oxygen as an electron sink forms the basis of another metabolic pathway—aerobic respiration. That pathway originally evolved in microorganisms and then was captured, through endosymbiosis, by other microorganisms, forming eukaryotic cells. Eukaryotic cells, the basis of all “complex” multicellular animal life, therefore, are the result of the shift of Earth’s metabolism to reliance on oxygen. The vast majority of carbon on Earth is stored in the lithosphere (the outer solid part of the Earth) in approximately a 4:1 ratio of inorganic carbon (carbonates) and organic matter. The organic matter represents a fraction of reducing equivalents (such as electrons) that have been removed through biological metabolism, thereby allowing oxidation of the Earth’s surface. On geological time scales the effect of biological metabolism on atmospheric CO2 may be outweighed by other sources. Significant variation in the CO2 content in Earth’s atmosphere is apparently primarily in response to tectonic activity (Berner, 2004). Nonbiological sources like volcanism can also have a major impact on atmospheric CO2 content. On a shorter time scale, however, CO2 concentration in the atmosphere is controlled primarily by exchange with the ocean and the biosphere (Falkowski et al., 2000). How metabolic pathways adjust to changes in CO2 on geological time scales remains unclear. Some microbial organisms are able to use several different metabolic pathways. Joshi and Tabita (1996) discovered a common regulatory circuit that regulates the balance between photosynthesis, respiration, and nitrogen fixation within these bacteria. In photosynthetic cells, the ultimate choice of metabolic pathway might lie in how the balance between chloroplasts and mitochondria is controlled (Nisbet and Fowler, 2005). This intriguing conjecture remains to be explored and tested but is of considerable importance to develop an understanding of the complex coupling of atmospheric carbon levels, individual organisms’ metabolisms, and the net effect of the metabolisms of entire communities.
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research Another area ripe for theoretical and conceptual breakthroughs is the role of microorganisms in the metabolism of plants and animals (Box 4-2). CROSS-CUTTING QUESTIONS IN METABOLISM Whole-organism metabolism can be described by simple molecular patterns of products, but the processes that shape these patterns remain poorly understood. One of the challenges of biology is establishing clear mechanistic links between structure and function. This challenge cuts across levels of organization. For example, understanding the effects of metabolism on how ecosystems work demands establishing connections between structure and function. Structure at this scale is defined as the composition and abundance of species, and function is defined as the integrated metabolism of a biological community, including respiration, primary productivity, decomposition rates, nitrification, denitrification, and other functions. Biologists have known for a long time that two variables have profound influence on an organism’s metabolic fluxes: body size and temperature. The effect of these two factors on a handful of metabolic functions (aerobic respiration) and in a handful of taxa (animals) has been carefully studied. The rate of aerobic respiration is known to be proportional to body size raised to an exponent. Respiration, like all metabolic processes, is also known to be dependent on temperature. The joint effect of body size and temperature on the rate of aerobic respiration can be described by the product of a power function of body size (called an allometric function) and the Arrhenius-Boltzmann equation, which relates the rate of biochemical reactions with temperature (Gillooly et al., 2001). A recent flurry of theoretical explorations attempts to explain not only the seeming universal dependence of aerobic respiration on body mass and temperature but also the putative ubiquity of the value of ¾ in the exponent of the power function that relates metabolic rate with body size. The theories have led to the conjecture that the value of this power is the consequence of the structure of the systems that distribute oxygen and nutrients in organisms (West et al., 1997). The theory has been extended to terrestrial vascular plants and has led to the remarkable prediction that both photosynthetic rate and respiration should also scale with plant mass to the ¾ power. This theoretical research has been accompanied by attempts to include these relationships in scaling exercises that predict ecosystem-level properties such as the metabolic balance of the oceans and the productivity and decomposition rates in terrestrial ecosystems (López-Urrutia et al., 2006). These calculations suggest that first-order estimates about the magnitude of these processes can be made from knowledge about the size
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research BOX 4-2 The Role of Microbial Communities in Metabolism To elucidate the structure of a biological community, biologists need to determine how many species there are and their relative abundances. Answering these questions is more difficult than it seems, especially for the microscopic organisms that constitute the metabolic backbone of most ecosystems. A large fraction of these microorganisms cannot be characterized by the traditional approach of isolation and culture. The techniques of metagenomics, as discussed in Box 3-2, make it possible to probe the structure of microbial communities and to link that structure with metabolic function. Metagenomics is also making it possible to explore the microbial communities that live on and in virtually all higher organisms. In fact, our theoretical understanding of metabolism now must incorporate the realization that all organisms—from plants to invertebrates to mammals—have an associated microbial community that affects many aspects of their physiology, including metabolism. The analysis of the metagenomes of various host-associated microbial communities has been used to diagnose functional metabolic differences among communities (Tringe et al., 2005). It also can be used to assess the spatial heterogeneity in metabolic function in a single community and its changes through time. For example, differences in the nutritional physiology among individuals of a single species might be shaped by differences in the metabolic capacities of their nutritional symbionts. Ruth Ley and her collaborators (Ley et al., 2006) recently found large differences in the composition of the microbial community of obese and lean people. In an accompanying study by the same group, Paul Turnbaugh (Turnbaugh et al., 2006) transferred the microbiota of obese mice to lean, microbe-free mice. These recipient mice extracted more calories from their food and gained slightly more fat than mice receiving microbiota from lean mice. Although these results should be interpreted cautiously (cause and effect are unclear), their results suggest that differences in the efficiency of caloric extraction from food might be determined by the composition of the gut’s microbiota. More generally, the results emphasize how the metabolic capacities of multicellular animals and plants are complemented, and sometimes extended greatly, by those of their symbiotic microbes. The implications of this complementarity are profound not only for the study of metabolism but also for the study of health, development, and evolution. There are many opportunities for the development of theories to explain and predict the impact of these microbial communities on multicellular organisms. Metagenomic surveys are one of the novel genomics-based approaches that will allow the empirical testing of such theories, opening up intriguing lines of scientific inquiry that will involve microbiologists with nutritionists, physiologists, and ecologists. Current technologies have been sufficient to show the tremendous promise of metagenomics approaches, but detailed understanding of microbial communities that may contain thousands of species will require significant advances. Most importantly, theoretical advances in understanding what controls community assembly, structure, and stability will be very important in guiding what technology to develop and what experiments to do.
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research distribution of the organisms that structure these ecosystems and from the temperature at which they operate. What has been called the metabolic theory of ecology has many detractors. The details of its theoretical foundation have been criticized, and the ubiquity and universality of the ¾-power rule have been challenged. Furthermore, the patterns revealed by the approach can have large errors around predicted values. Although the theory undoubtedly has limitations, it is a bold and promising attempt. The ubiquity of the power functions relating metabolic function to body size and the importance of temperature for biological processes are undeniable. The challenge is not to dismiss the theory but to test it, find the cases in which it fails, and modify and strengthen it to improve its power. The task is to explain not only the general trends in these size-temperature-metabolism relationships but also the details that make some systems deviate from them. The metabolic theory has to be linked to the molecular details of the metabolic architectures of living systems. The magnitude of an organism’s metabolism is the outcome of feedback between the “the whole,” construed as the whole organism, and “the parts,” construed as the cellular and subcellular machinery. Does a mitochondrion “know” that it is within a mouse or an elephant and behave differently in a predictable manner? Since a large fraction of the functional proteins come from the nuclear genome, there is a strong basis for such coupling. The nature of these feedbacks remains unclear and is a fertile area of investigation. A complete metabolic theory would link the details of the structure of metabolic pathways in cells and organelles with the “macro” patterns that biologists can discern and that the metabolic theory aims to explain. Biologists are still far from this goal. Although a metabolic theory of life is still being constructed, the metabolic theory of ecology has forced biologists to attempt to search for simplicity in the patterns produced by seemingly complex processes and has given a glimpse of hope about the feasibility of the task. Although the conservation of metabolic pathways is clear, some surprises have emerged in recent years in relation to size-temperature-metabolism relationships. One is the discovery of extremely slowly growing microorganisms deep in Earth’s sediments (D’Hondt et al., 2002). Those organisms grow so slowly that it is virtually impossible to measure gas exchange with their environment, yet they are not small compared to other microorganisms. In contrast, the discovery of deep-sea hydrothermal vents revealed the presence of symbiotic chemoautotrophic bacteria associated with numerous invertebrates (animals), living near very high temperature, sulfide-rich waters emanating from marine volcanoes. Those two examples suggest that the temperature-size-metabolic rate relationships derived from observations of metazoans and higher plants probably cannot be extrapolated to microbial communities. Yet the basic thermodynamic processes that
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research control metabolic rates viz. temperature still apply. Clearly, the “anomalies” suggest that the patterns so far discerned are not universal and that investment in further theoretical work to understand these relationships would be highly productive. CONCLUSION Systems geobiology and such approaches as metagenomics cut across traditional disciplinary boundaries. Answering the questions they pose requires the combined skills of physical scientists (including computer scientists, physicists, and chemists) and biologists. For example, global metabolic fluxes are the cumulative result of the specific capabilities of individual molecules, powering individual cells in different organisms, which themselves interact in many different communities. Thus, a deep understanding of these fluxes will require input from fields as diverse as enzymology, protein chemistry, cell biology, biophysics, comparative physiology, and ecology, just to list some of the necessary biologists’ areas of expertise. Understanding the biosphere’s metabolism will require that technologies developed to measure metabolic processes at small scales be refined and scaled up to appropriately broad temporal and spatial scales. These technologies include combining stable isotope and gas-exchange measurements with remote sensing and mathematical modeling. So far, the study of Earth’s metabolism has been based on the theoretical frameworks provided by thermodynamics and the laws of chemical equilibrium. The next chapter discusses the problem that in order to understand how cells really work, biologists will need to complement these frameworks with other approaches that are more realistic at the scale of cells. It may be that a more accurate understanding of cell metabolism will contribute to a better understanding of the planet’s metabolism. This observation emphasizes that the practitioners of this new science have to work comfortably across scales—from genomics to the atmospheric sciences through cell and organismal biology. The broadly integrative training approach of the physiological sciences might be invaluable to train students of Earth’s “physiology,” such as the biological, geological, and atmospheric processes that facilitate global biogeochemical fluxes of elements and maintain this planet far from thermodynamic equilibrium. Deep understanding of the processes and interactions that couple the biosphere and the geosphere has tremendous potential to generate solutions to societal problems. For example, one question that could be addressed is “Which key biological reactions, if catalyzed on an industrial scale, would make the transition to sustainability?” Clearly the photochemical splitting of water would potentially provide hydrogen as an infinite energy carrier, and therefore can potentially negate the need for combusting fossil fuels.
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The Role of Theory in Advancing 21st-Century Biology: Catalyzing Transformative Research Similarly, the ability to fix N2 efficiently would alter the impending crisis of eutrophication of coastal waters throughout the world. Over the past century, humans have dramatically altered the global environment, extracting resources and energy to facilitate economic growth and development. Many valuable resources, such as fixed inorganic nitrogen and organic carbon, are essential for production of food and for fuels. These biologically critical molecules are either produced inefficiently by chemical synthesis or are not available in sufficient quantities. Over the next century, a major challenge for society will be to develop or redesign metabolic pathways, based primarily on microbial systems, to greatly accelerate fluxes of materials and energy. One of the major outcomes of understanding metabolic pathways and energy transformation processes is to replace technologies designed in the 19th and 20th centuries with sustainable processes that are biologically driven.