Evolution Of Metabolism Research Articles

Overlooked and misunderstood: can glutathione conjugates be clues to understanding plant glutathione transferases?

Plant glutathione transferases (GSTs) constitute a large and diverse family of enzymes that are involved in plant stress response, metabolism and defence, yet their physiological functions remain largely elusive. Consistent with the traditional view on GSTs across organisms as detoxification enzymes, in vitro most plant GSTs catalyse glutathionylation, conjugation of the tripeptide glutathione (GSH; γ-Glu-Cys-Gly) onto reactive molecules. However, when it comes to elucidating GST functions, it remains a key challenge that the endogenous plant glutathione conjugates (GS-conjugates) that would result from such glutathionylation reactions are rarely reported. Furthermore, GSTs often display high substrate promiscuity, and their proposed substrates are prone to spontaneous chemical reactions with GSH; hence, single-gene knockouts rarely provide clear chemotypes or phenotypes. In a few cases, GS-conjugates are demonstrated to be biosynthetic intermediates that are rapidly further metabolized towards a pathway end product, explaining their low abundance and rare detection. In this review, we summarize the current knowledge of plant GST functions and how and possibly why evolution has resulted in a broad and extensive expansion of the plant GST family. Finally, we demonstrate that endogenous GS-conjugates are more prevalent in plants than assumed and suggest they are overlooked as clues towards the identification of plant GST functions. This article is part of the theme issue 'The evolution of plant metabolism'.

Biotic interactions, evolutionary forces and the pan-plant specialized metabolism.

Plant specialized metabolism has a complex evolutionary history. Some aspects are conserved across the green lineage, but many metabolites are unique to certain lineages. The network of specialized metabolism continuously diversified, simplified or reshaped during the evolution of streptophytes. Many routes of pan-plant specialized metabolism are involved in plant defence. Biotic interactions are recalled as major drivers of lineage-specific metabolomic diversification. However, the consequences of this diversity of specialized metabolism in the context of plant terrestrialization and land plant diversification into the major lineages of bryophytes, lycophytes, ferns, gymnosperms and angiosperms remain only little explored. Overall, this hampers conclusions on the evolutionary scenarios that shaped specialized metabolism. Recent efforts have brought forth new streptophyte model systems, an increase in genetically accessible species from distinct major plant lineages, and new functional data from a diversity of land plants on specialized metabolic pathways. In this review, we will integrate the recent data on the evolution of the plant immune system with the molecular data of specialized metabolism and its recognition. Based on this we will provide a contextual framework of the pan-plant specialized metabolism, the evolutionary aspects that shape it and the impact on adaptation to the terrestrial environment.This article is part of the theme issue 'The evolution of plant metabolism'.

The evolution of plant responses underlying specialized metabolism in host-pathogen interactions.

In the course of plant evolution from aquatic to terrestrial environments, land plants (embryophytes) acquired a diverse array of specialized metabolites, including phenylpropanoids, flavonoids and cuticle components, enabling adaptation to various environmental stresses. While embryophytes and their closest algal relatives share candidate enzymes responsible for producing some of these compounds, the complete genetic network for their biosynthesis emerged in embryophytes. In this review, we analysed genomic data from chlorophytes, charophytes and embryophytes to identify genes related to phenylpropanoid, flavonoid and cuticle biosynthesis. By integrating published research, transcriptomic data and metabolite studies, we provide a comprehensive overview on how these specialized metabolic pathways have contributed to plant defence responses to pathogens in non-vascular bryophytes and vascular plants throughout evolution. The evidence suggests that these biosynthetic pathways have provided land plants with a repertoire of conserved and lineage-specific compounds, which have shaped immunity against invading pathogens. The discovery of additional enzymes and metabolites involved in bryophyte responses to pathogen infection will provide evolutionary insights into these versatile pathways and their impact on environmental terrestrial challenges.This article is part of the theme issue 'The evolution of plant metabolism'.

The evolution of flavonoid biosynthesis.

The flavonoid pathway is characteristic of land plants and a central biosynthetic component enabling life in a terrestrial environment. Flavonoids provide tolerance to both abiotic and biotic stresses and facilitate beneficial relationships, such as signalling to symbiont microorganisms, or attracting pollinators and seed dispersal agents. The biosynthetic pathway shows great diversity across species, resulting principally from repeated biosynthetic gene duplication and neofunctionalization events during evolution. Such events may reflect a selection for new flavonoid structures with novel functions that enable occupancy of varied ecological niches. However, the biochemical and genetic diversity of the pathway also likely resulted from evolution along parallel trends across land plant lineages, producing variant compounds with similar biological functions. Analyses of the wide range of whole-plant genome sequences now available, particularly for archegoniate plants, have enabled proposals on which genes were ancestral to land plants and which arose within the land plant lineages. In this review, we discuss the emerging proposals for how the flavonoid pathway may have evolved and diversified. This article is part of the theme issue 'The evolution of plant metabolism'.

A Methodology to Measure Glucose Metabolism by Quantitative Analysis of PET Images.

Positron emission tomography (PET) with F-18 fluorodeoxyglucose (FDG) tracer is the standard clinical technique to measure myocardial and vessel metabolism and viability and to investigate the metabolic syndrome associated with cardiovascular diseases. The quantitative analysis of PET images allows one to study the cardiovascular physiological processes, by extracting quantitative parameters from the analysis of the tracer kinetic. Here, we propose a new methodology to quantify and evaluate the evolution of glucose metabolism inside the myocardium and the large vascular structures over time. We merge and analyze PET and CT cardiac images, extracting different volumes of interest (VOI) and performing quantitative measurements. To validate it, we apply the methodology to merge images of the aorta vessel for patients affected by metabolic syndrome. The application of the proposed approach to the use case reveals a correlation between administered drugs and metabolic syndrome, measuring the glucose metabolic rate (MRGlu) in both the myocardium and aorta. The proposed methodology can be used to evaluate some cardiovascular risk indexes of diabetic patients, too. The proposed methodology can also be deployed to analyze other application domains.

Abstract IA-09: Spatiotemporal metabolic networks in pancreatic cancer and associated cachexia

Abstract Cachexia or body wasting is a significant contributing factor to the morbidity and mortality of pancreatic cancer. Despite an unmet need, its metabolic underpinnings remain poorly understood. Here, we characterize an inducible mouse model of pancreatic cancer cachexia that recaptures human disease progression. We present longitudinal systemic metabolic profiling analyses through pre-, early and late cachexia stages in male and female pancreas, its interstitial fluid (IF), plasma, liver, adipose and skeletal muscle. We find that each tissue has a unique metabolome and trajectory across stages, and reveal metabolic signatures with marked lipid enrichment in the pancreatic IF. Using mathematical modeling, we identify metabolites participating in cross-tissue networks and in vivo validate a lactate-hexose connection. We find systemic metabolic changes prior to weight loss, and use feature selection algorithms to identify potential predictive markers of cachexia progression. Our study provides a resource for system-wide metabolic network evolution of pancreatic cancer cachexia, highlighting the potential for prevention and therapy. Citation Format: Blanca Majem, Min-Sik Lee, Kyung Cheul Shin, Insia Naqvi, Courtney Dennis, Lucas Dailey, Sarah Jeanfavre, Mari Mino-Kenudson, Joao B Xavier, Clary B Clish, Deepti Mathur, Nada Y Kalaany. Spatiotemporal metabolic networks in pancreatic cancer and associated cachexia [abstract]. In: Proceedings of the AACR Special Conference in Cancer Research: Advances in Pancreatic Cancer Research; 2024 Sep 15-18; Boston, MA. Philadelphia (PA): AACR; Cancer Res 2024;84(17 Suppl_2):Abstract nr IA-09.

Functional evolution and diversification of CYP82D subfamily members have shaped flavonoid diversification in the genus Scutellaria

Flavonoids, the largest class of polyphenols, exhibit substantial structural and functional diversity, yet their evolutionary diversification and specialized functions remain largely unexplored. The genus Scutellaria is notable for its rich flavonoid diversity, particularly of 6/8-hydroxylated variants biosynthesized by the cytochrome P450 subfamily CYP82D. Our study analyzes metabolic differences between Scutellaria baicalensis and Scutellaria barbata, and the results suggest that CYP82Ds have acquired a broad range of catalytic functions over their evolution. By integrating analyses of metabolic networks and gene evolution across 22 Scutellaria species, we rapidly identified 261 flavonoids and delineated five clades of CYP82Ds associated with various catalytic functions. This approach revealed a unique catalytic mode for 6/8-hydroxylation of flavanone substrates and the first instance of 7-O-demethylation of flavonoid substrates catalyzed by a cytochrome P450. Ancestral sequence reconstruction and functional validation demonstrated that gradual neofunctionalization of CYP82Ds has driven the chemical diversity of flavonoids in the genus Scutellaria throughout its evolutionary history. These findings enhance our understanding of flavonoid diversity, reveal the intricate roles of CYP82Ds in Scutellaria species, and highlight the extensive catalytic versatility of cytochrome P450 members within plant taxa.

Metabolic evolution and bottleneck insights into simultaneous autotroph-heterotroph anammox system for real municipal wastewater nitrogen removal

When biological nitrogen removal (BNR) systems shifted from treating simulated wastewater to real wastewater, a microbial succession occurred, often resulting in a decline in efficacy. Notably, despite their high nitrogen removal efficiency for real wastewater, anammox coupled systems operating without or with minimal carbon sources also exhibited a certain degree of performance reduction. The underlying reasons and metabolic shifts within these systems remained elusive. In this study, the simultaneous autotrophic/heterotrophic anammox system demonstrated remarkable metabolic resilience upon exposure to real municipal wastewater, achieving a nitrogen removal efficiency (NRE) of 82.83 ± 2.29 %. This resilience was attributed to the successful microbial succession and the complementary metabolic functions of heterotrophic microorganisms, which fostered a resilient microbial community. The system's ability to harness multiple electron sources, including NADH oxidation, the TCA cycle, and organics metabolism, allowed it to establish a stable and efficient electron transfer chain, ensuring effective nitrogen removal. Despite the denitrification channel's nitrite supply capability, the analysis of the interspecies correlation network revealed that the synergistic metabolism between AOB and AnAOB was not fully restored, resulting in selective functional bacterial and genetic interactions and the system's PN/A performance declined. Additionally, the enhanced electron affinity of PD increased interconversion of NO3−-N and NO2−-N, limiting the efficient utilization of electrons and thereby constraining nitrogen removal performance. This study elucidated the metabolic mechanism of nitrogen removal limitations in anammox-based systems treating real municipal wastewater, enhancing our understanding of the metabolic functions and electron transfer within the symbiotic bacterial community.

CYP76BK1 orthologs catalyze furan and lactone ring formation in clerodane diterpenoids across the mint family.

The Lamiaceae (mint family) is the largest known source of furanoclerodanes, a subset of clerodane diterpenoids with broad bioactivities including insect antifeedant properties. The Ajugoideae subfamily, in particular, accumulates significant numbers of structurally related furanoclerodanes. The biosynthetic capacity for formation of these diterpenoids is retained across most Lamiaceae subfamilies, including the early-diverging Callicarpoideae which forms a sister clade to the rest of Lamiaceae. VacCYP76BK1, a cytochrome P450 monooxygenase from Vitex agnus-castus, was previously found to catalyze the formation of the proposed precursor to furan and lactone-containing labdane diterpenoids. Through transcriptome-guided pathway exploration, we identified orthologs of VacCYP76BK1 in Ajuga reptans and Callicarpa americana. Functional characterization demonstrated that both could catalyze the oxidative cyclization of clerodane backbones to yield a furan ring. Subsequent investigation revealed a total of ten CYP76BK1 orthologs across six Lamiaceae subfamilies. Through analysis of available chromosome-scale genomes, we identified four CYP76BK1 members as syntelogs within a conserved syntenic block across divergent subfamilies. This suggests an evolutionary lineage that predates the speciation of the Lamiaceae. Functional characterization of the CYP76BK1 orthologs affirmed conservation of function, as all catalyzed furan ring formation. Additionally, some orthologs yielded two novel lactone ring moieties. The presence of the CYP76BK1 orthologs across Lamiaceae subfamilies closely overlaps with the distribution of reported furanoclerodanes. Together, the activities and distribution of the CYP76BK1 orthologs identified here support their central role in furanoclerodane biosynthesis within the Lamiaceae family. Our findings lay the groundwork for biotechnological applications to harness the economic potential of this promising class of compounds.

Carbon metabolism mechanisms and evolution characteristics analysis of the food-water-energy nexus system under blue-green infrastructure changes

Food, water, and energy comprise a complex system (FWE nexus) that generates much carbon emissions during operation. At the same time, urban blue-green infrastructure (BGI) has a critical carbon sequestration function. This paper combines the functions of the FWE nexus and BGI and uses ecological network analysis (ENA) and the Markov model to measure the carbon metabolism (CM) mechanisms and evolutionary characteristics of BGI and FWE nexus (BGI-FWE nexus) complex systems. The results show that Guangzhou has high carbon emissions, and Zhaoqing and Huizhou have high carbon sequestration. Resident land and industrial and transportation land transfers to different land uses are more likely to produce positive carbon flows, while BGI transfers to other types are more likely to produce negative carbon flows. The study of CM mechanisms reveals a high proportion of competition relationships and a low proportion of mutualism relationships. The ecological utility index (EUI) tends to fall initially and then increase, peaking at 0.84 in 2015–2020, the highest value for the study period. The CM network has less system robustness (SR) and is in an unsustainable state of high redundancy and low efficiency. The mechanism evolution characterization study’s findings show a decreased likelihood of remaining original and less stability in the spatial transfer probability matrices of EUI and SR. In this study, we constructed a BGI-FWE nexus research framework based on the different CM functions of BGI and FWE nexus. The research framework contributes to the realization of carbon reduction in the FWE nexus system and is essential for the planning and management of urban BGI.

Evolution of multi-scale structure and microbiota metabolism of lentil resistant starch during the dynamic fermentation in vitro

This study investigated the structural changes of resistant starch (RS) derived from autoclaved lentil starch (ALRS) and untreated lentil starch (ULRS) during in vitro colonic fermentation, as well as their regulatory effects on the composition of the intestinal microbiota. Following in vitro fermentation, both RS samples exhibited a progressive decrease in molecular weight and a gradual increase in double helix/order. Bifidobacterium was more abundant in ULRS during the initial period of fermentation, while ALRS showed higher abundance in the later stage. ALRS demonstrated greater production of short-chain fatty acids (SCFAs) compared to ULRS, likely attributed to its higher structural order and faster fermentation pattern. The distinct surface morphologies of ULRS and ALRS played a crucial role in determining the accessibility of RS substrates for microbial fermentation. These different structural patterns also influenced the shifts in microbial composition in fecal cultures, leading to variations in SCFAs production through anaerobic fermentation.

Hyperpolarized Magnetic Resonance Imaging, Nuclear Magnetic Resonance Metabolomics, and Artificial Intelligence to Interrogate the Metabolic Evolution of Glioblastoma.

Glioblastoma (GBM) is a malignant Grade VI cancer type with a median survival duration of only 8-16 months. Earlier detection of GBM could enable more effective treatment. Hyperpolarized magnetic resonance spectroscopy (HPMRS) could detect GBM earlier than conventional anatomical MRI in glioblastoma murine models. We further investigated whether artificial intelligence (A.I.) could detect GBM earlier than HPMRS. We developed a deep learning model that combines multiple modalities of cancer data to predict tumor progression, assess treatment effects, and to reconstruct in vivo metabolomic information from ex vivo data. Our model can detect GBM progression two weeks earlier than conventional MRIs and a week earlier than HPMRS alone. Our model accurately predicted in vivo biomarkers from HPMRS, and the results inferred biological relevance. Additionally, the model showed potential for examining treatment effects. Our model successfully detected tumor progression two weeks earlier than conventional MRIs and accurately predicted in vivo biomarkers using ex vivo information such as conventional MRIs, HPMRS, and tumor size data. The accuracy of these predictions is consistent with biological relevance.

Biofluorescence imaging-guided spatial metabolic tracing: In vivo tracking of metabolic activity in circulating tumor cell-mediated multi-organ metastases

Circulating tumor cells (CTC) are considered metastatic precursors that are shed from the primary or metastatic deposits and navigate the bloodstream before undergoing extravasation to establish distant metastases. Metabolic reprogramming appears to be a hallmark of metastatic progression, yet current methods for evaluating metabolic heterogeneity within organ-specific metastases in vivo are limited. To overcome this challenge, we present Biofluorescence Imaging-Guided Spatial Metabolic Tracing (BIGSMT), a novel approach integrating in vivo biofluorescence imaging, stable isotope tracing, stain-free laser capture microdissection, and liquid chromatography-mass spectrometry. This innovative technology obviates the need for staining or intricate sample preparation, mitigating metabolite loss, and substantially enhances detection sensitivity and accuracy through chemical derivatization of polar metabolites in central carbon pathways. Application of BIGSMT to a preclinical CTC-mediated metastasis mouse model revealed significant heterogeneity in the in vivo carbon flux from glucose into glycolysis and the tricarboxylic acid (TCA) cycle across distinct metastatic sites. Our analysis indicates that carbon predominantly enters the TCA cycle through the enzymatic reaction catalyzed by pyruvate dehydrogenase. Thus, our spatially resolved BIGSMT technology provides fresh insights into the metabolic heterogeneity and evolution during melanoma CTC-mediated metastatic progression and points to novel therapeutic opportunities.

Genomic insights into the evolution of secondary metabolism of Escovopsis and its allies, specialized fungal symbionts of fungus-farming ants.

The metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, symbionts in the gardens of fungus-farming ants. We ask how the gain and loss of various biosynthetic pathways correspond to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes composed of seven to eight chromosomes. The genomes are highly syntenic with macrosynteny decreasing with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. An ancestral state reconstruction analysis of biosynthetic pathways revealed that, while many secondary metabolites are shared with non-ant-associated Sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their fungal hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system.IMPORTANCEMicrobial symbionts interact with their hosts and competitors through a remarkable array of secondary metabolites and natural products. Here, we highlight the highly streamlined genomic features of attine-associated fungal symbionts. The genomes of Escovopsis species, as well as species from other symbiont genera, many of which are common with the gardens of fungus-growing ants, are defined by seven chromosomes. Despite a high degree of metabolic conservation, we observe some variation in the symbionts' potential to produce secondary metabolites. As the phylogenetic distribution of the encoding biosynthetic gene clusters coincides with attine transitions in agricultural systems, we highlight the likely role of these metabolites in mediating adaptation by a group of highly specialized symbionts.

Oomycete Metabolism Is Highly Dynamic and Reflects Lifestyle Adaptations.

The selective pressure of pathogen-host symbiosis drives adaptations. How these interactions shape the metabolism of pathogens is largely unknown. Here, we use comparative genomics to systematically analyze the metabolic networks of oomycetes, a diverse group of eukaryotes that includes saprotrophs as well as animal and plant pathogens, with the latter causing devastating diseases with significant economic and/or ecological impacts. In our analyses of 44 oomycete species, we uncover considerable variation in metabolism that can be linked to lifestyle differences. Comparisons of metabolic gene content reveal that plant pathogenic oomycetes have a bipartite metabolism consisting of a conserved core and an accessory set. The accessory set can be associated with the degradation of defense compounds produced by plants when challenged by pathogens. Obligate biotrophic oomycetes have smaller metabolic networks, and taxonomically distantly related biotrophic lineages display convergent evolution by repeated gene losses in both the conserved as well as the accessory set of metabolisms. When investigating to what extent the metabolic networks in obligate biotrophs differ from those in hemibiotrophic plant pathogens, we observe that the losses of metabolic enzymes in obligate biotrophs are not random and that gene losses predominantly influence the terminal branches of the metabolic networks. Our analyses represent the first metabolism-focused comparison of oomycetes at this scale and will contribute to a better understanding of the evolution of oomycete metabolism in relation to lifestyle adaptation. Numerous oomycete species are devastating plant pathogens that cause major damage in crops and natural ecosystems. Their interactions with hosts are shaped by strong selection, but how selection affects adaptation of the primary metabolism to a pathogenic lifestyle is not yet well established. By pan-genome and metabolic network analyses of distantly related oomycete pathogens and their nonpathogenic relatives, we reveal considerable lifestyle- and lineage-specific adaptations. This study contributes to a better understanding of metabolic adaptations in pathogenic oomycetes in relation to lifestyle, host, and environment, and the findings will help in pinpointing potential targets for disease control. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Introducing carbon assimilation in yeasts using photosynthetic directed endosymbiosis

Conversion of heterotrophic organisms into partially or completely autotrophic organisms is primarily accomplished by extensive metabolic engineering and laboratory evolution efforts that channel CO2 into central carbon metabolism. Here, we develop a directed endosymbiosis approach to introduce carbon assimilation in budding yeasts. Particularly, we engineer carbon assimilating and sugar-secreting photosynthetic cyanobacterial endosymbionts within the yeast cells, which results in the generation of yeast/cyanobacteria chimeras that propagate under photosynthetic conditions in the presence of CO2 and in the absence of feedstock carbon sources like glucose or glycerol. We demonstrate that the yeast/cyanobacteria chimera can be engineered to biosynthesize natural products under the photosynthetic conditions. Additionally, we expand our directed endosymbiosis approach to standard laboratory strains of yeasts, which transforms them into photosynthetic yeast/cyanobacteria chimeras. We anticipate that our studies will have significant implications for sustainable biotechnology, synthetic biology, and experimentally studying the evolutionary adaptation of an additional organelle in yeast.

Convergent evolution toward a slow pace of life predisposes insular endotherms to anthropogenic extinctions.

Island vertebrates have evolved a number of morphological, physiological, and life history characteristics that set them apart from their mainland relatives. However, to date, the evolution of metabolism and its impact on the vulnerability to extinction of insular vertebrates remains poorly understood. This study used metabolic data from 2813 species of tetrapod vertebrates, including 695 ectothermic and 2118 endothermic species, to reveal that island mammals and birds evolved convergent metabolic strategies toward a slow pace of life. Insularity was associated with shifts toward slower metabolic rates and greater generation lengths in endotherms, while insularity just drove the evolution of longer generation lengths in ectotherms. Notably, a slow pace of life has exacerbated the extinction of insular endemic species in the face of anthropogenic threats. These findings have important implications for understanding physiological adaptations associated with the island syndrome and formulating conservation strategies across taxonomic groups with different metabolic modes.

Impact of steroid biosynthesis on the aerobic adaptation ofeukaryotes.

Steroids are indispensable components of the eukaryotic cellular membrane and the acquisition of steroid biosynthesis was a key factor that enabled the evolution of eukaryotes. The polycyclic carbon structures of steroids can be preserved in sedimentary rocks as chemical fossils for billions of years and thus provide invaluable clues to trace eukaryotic evolution from the distant past. Steroid biosynthesis consists of (1) the production of protosteroids and (2) the subsequent modifications toward "modern-type" steroids such as cholesterol and stigmasterol. While protosteroid biosynthesis requires only two genes for the cyclization of squalene, complete modification of protosteroids involves ~10 additional genes. Eukaryotes universally possess at least some of those additional genes and thus produce modern-type steroids as major final products. The geological biomarker records suggest a prolonged period of solely protosteroid production in the mid-Proterozoic before the advent of modern-type steroids in the Neoproterozoic. It has been proposed that mid-Proterozoic protosteroids were produced by hypothetical stem-group eukaryotes that presumably possessed genes only for protosteroid production, even though in modern environments protosteroid production as a final product is found exclusively in bacteria. The host identity of mid-Proterozoic steroid producers is crucial for understanding the early evolution of eukaryotes. In this perspective, we discuss how geological biomarker data and genetic data complement each other and potentially provide a more coherent scenario for the evolution of steroids and associated early eukaryotes. We further discuss the potential impacts that steroids had on the evolution of aerobic metabolism in eukaryotes, which may have been an important factor for the eventual ecological dominance of eukaryotes in many modern environments.

Oxygenation of Earth's atmosphere induced metabolic and ecologic transformations recorded in the Lomagundi-Jatuli carbon isotopic excursion.

The oxygenation of Earth's atmosphere represents the quintessential transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution; molecular clock models indicate the diversification and ecological expansion of respiratory metabolisms in the several hundred million years following atmospheric oxygenation. Across this same interval, the geological record preserves 13C enrichment in some carbonate rocks, called the Lomagundi-Jatuli excursion (LJE). By combining data from geologic and genomic records, a self-consistent metabolic evolution model emerges for the LJE. First, fermentation and methanogenesis were major processes remineralizing organic carbon before atmospheric oxygenation. Once an ozone layer formed, shallow water and exposed environments were shielded from UVB/C radiation, allowing the expansion of cyanobacterial primary productivity. High primary productivity and methanogenesis led to preferential removal of 12C into organic carbon and CH4. Extreme and variable 13C enrichments in carbonates were caused by 13C-depleted CH4 loss to the atmosphere. Through time, aerobic respiration diversified and became ecologically widespread, as did other new metabolisms. Respiration displaced fermentation and methanogenesis as the dominant organic matter remineralization processes. As CH4 loss slowed, dissolved inorganic carbon in shallow environments was no longer highly 13C enriched. Thus, the loss of extreme 13C enrichments in carbonates marks the establishment of a new microbial mat ecosystem structure, one dominated by respiratory processes distributed along steep redox gradients. These gradients allowed the exchange of metabolic by-products among metabolically diverse organisms, providing novel metabolic opportunities. Thus, the microbially induced oxygenation of Earth's atmosphere led to the transformation of microbial ecosystems, an archetypal example of planetary microbiology.IMPORTANCEThe oxygenation of Earth's atmosphere represents the most extensive known chemical transformation of a planetary surface by microbial processes. In turn, atmospheric oxygenation transformed metabolic evolution by providing oxidants independent of the sites of photosynthesis. Thus, the evolutionary changes during this interval and their effects on planetary-scale biogeochemical cycles are fundamental to our understanding of the interdependencies among genomes, organisms, ecosystems, elemental cycles, and Earth's surface chemistry through time.

Atomically Resolved Transition Pathways of Iron Redox.

The redox transition between iron and its oxides is of the utmost importance in heterogeneous catalysis, biological metabolism, and geological evolution. The structural characteristics of this reaction may vary based on surrounding environmental conditions, giving rise to diverse physical scenarios. In this study, we explore the atomic-scale transformation of nanosized Fe3O4 under ambient-pressure H2 gas using in-situ environmental transmission electron microscopy. Our results reveal that the internal solid-state reactions dominated by iron diffusion are coupled with the surface reactions involving gaseous O or H species. During reduction, we observe two competitive reduction pathways, namely Fe3O4 → FeO → Fe and Fe3O4 → Fe. An intermediate phase with vacancy ordering is observed during the disproportionation reaction of Fe2+ → Fe0 + Fe3+, which potentially alleviates stress and facilitates ion migration. As the temperature decreases, an oxidation process occurs in the presence of environmental H2O and trace amounts of O2. A direct oxidation of Fe to Fe3O4 occurs in the absence of the FeO phase, likely corresponding to a change in the water vapor content in the atmosphere. This work elucidates a full dynamical scenario of iron redox under realistic conditions, which is critical for unraveling the intricate mechanisms governing the solid-solid and solid-gas reactions.