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Greening, Chris (Ed.)ABSTRACT Aerobes require dioxygen (O2) to grow; anaerobes do not. However, nearly all microbes—aerobes, anaerobes, and facultative organisms alike—express enzymes whose substrates include O2, if only for detoxification. This presents a challenge when trying to assess which organisms are aerobic from genomic data alone. This challenge can be overcome by noting that O2utilization has wide-ranging effects on microbes: aerobes typically have larger genomes encoding distinctive O2-utilizing enzymes, for example. These effects permit high-quality prediction of O2utilization from annotated genome sequences, with several models displaying ≈80% accuracy on a ternary classification task for which blind guessing is only 33% accurate. Since genome annotation is compute-intensive and relies on many assumptions, we asked if annotation-free methods also perform well. We discovered that simple and efficient models based entirely on genomic sequence content—e.g., triplets of amino acids—perform as well as intensive annotation-based classifiers, enabling rapid processing of genomes. We further show that amino acid trimers are useful because they encode information about protein composition and phylogeny. To showcase the utility of rapid prediction, we estimated the prevalence of aerobes and anaerobes in diverse natural environments cataloged in the Earth Microbiome Project. Focusing on a well-studied O2gradient in the Black Sea, we found quantitative correspondence between local chemistry (O2:sulfide concentration ratio) and the composition of microbial communities. We, therefore, suggest that statistical methods like ours might be used to estimate, or “sense,” pivotal features of the chemical environment using DNA sequencing data.IMPORTANCEWe now have access to sequence data from a wide variety of natural environments. These data document a bewildering diversity of microbes, many known only from their genomes. Physiology—an organism’s capacity to engage metabolically with its environment—may provide a more useful lens than taxonomy for understanding microbial communities. As an example of this broader principle, we developed algorithms that accurately predict microbial dioxygen utilization directly from genome sequences without annotating genes, e.g., by considering only the amino acids in protein sequences. Annotation-free algorithms enable rapid characterization of natural samples, highlighting quantitative correspondence between sequences and local O2levels in a data set from the Black Sea. This example suggests that DNA sequencing might be repurposed as a multi-pronged chemical sensor, estimating concentrations of O2and other key facets of complex natural settings.more » « less
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Our planet is a self-sustaining ecosystem powered by light energy from the sun, but roughly closed to matter. Many ecosystems on Earth are also approximately closed to matter and recycle nutrients by self-organizing stable nutrient cycles, e.g., microbial mats, lakes, open ocean gyres. However, existing ecological models do not exhibit the self-organization and dynamical stability widely observed in such planetary-scale ecosystems. Here, we advance a conceptual model that explains the self-organization, stability, and emergent features of closed microbial ecosystems. Our model incorporates the bioenergetics of metabolism into an ecological framework. By studying this model, we uncover a crucial thermodynamic feedback loop that enables metabolically diverse communities to almost always stabilize nutrient cycles. Surprisingly, highly diverse communities self-organize to extract 10 of the maximum extractable energy, or 100 fold more than randomized communities. Further, with increasing diversity, distinct ecosystems show strongly correlated fluxes through nutrient cycles. However, as the driving force from light increases, the fluxes of nutrient cycles become more variable and species-dependent. Our results highlight that self-organization promotes the efficiency and stability of complex ecosystems at extracting energy from the environment, even in the absence of any centralized coordination.more » « less
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Significance Metabolism relies on a small class of molecules (coenzymes) that serve as universal donors and acceptors of key chemical groups and electrons. Although metabolic networks crucially depend on structurally redundant coenzymes [e.g., NAD(H) and NADP(H)] associated with different enzymes, the criteria that led to the emergence of this redundancy remain poorly understood. Our combination of modeling and structural and sequence analysis indicates that coenzyme redundancy may not be essential for metabolism but could rather constitute an evolved strategy promoting efficient usage of enzymes when biochemical reactions are near equilibrium. Our work suggests that early metabolism may have operated with fewer coenzymes and that adaptation for metabolic efficiency may have driven the rise of coenzyme diversity in living systems.more » « less
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ver the last 10,000 years, human activities have transformed Earth through farming, forestry, mining, and industry. The complex results of these activities are now observed and quantified as “human impacts” on Earth’s atmosphere, oceans, biosphere, and geochemistry. While myriad studies have explored facets of human impacts on the planet, they are necessarily technical and often highly focused. Thus, finding reliable quantitative information requires a significant investment of time to assess each quantity and associated uncertainty. We present the Human Impacts Database (www.anthroponumbers.org), which houses a diverse array of such quantities. We review a subset of these values and how they help build intuition for understanding the Earth-human system. While collation alone does not tell us how to best ameliorate human impacts, we contend that any future plans should be made in light of a quantitative understanding of the interconnected ways in which humans influence the planet.more » « less
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null (Ed.)Many photosynthetic organisms employ a CO 2 concentrating mechanism (CCM) to increase the rate of CO 2 fixation via the Calvin cycle. CCMs catalyze ≈50% of global photosynthesis, yet it remains unclear which genes and proteins are required to produce this complex adaptation. We describe the construction of a functional CCM in a non-native host, achieved by expressing genes from an autotrophic bacterium in an Escherichia coli strain engineered to depend on rubisco carboxylation for growth. Expression of 20 CCM genes enabled E. coli to grow by fixing CO 2 from ambient air into biomass, with growth in ambient air depending on the components of the CCM. Bacterial CCMs are therefore genetically compact and readily transplanted, rationalizing their presence in diverse bacteria. Reconstitution enabled genetic experiments refining our understanding of the CCM, thereby laying the groundwork for deeper study and engineering of the cell biology supporting CO 2 assimilation in diverse organisms.more » « less
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