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DOE OSTI2019

Fungal endophytes of Populus trichocarpa alter host phenotype, gene expression and rhizobiome composition

Mortierella and Ilyonectria include common species of soil fungi which are frequently detected as root endophytes in many plants including Populus spp. However, the ecological roles of these and other endophytic fungi with respect to plant growth and function are still not well understood. The functional ecology of two key taxa from the Populus rhizobiome, Mortierella elongata PMI93 and Ilyonectria europaea PMI82, was studied by coupling forest soil bioassays with environmental metatranscriptomics. Using soil bioassay experiments amended with fungal inoculants, M. elongata was observed to promote the growth of Populus. Here, this response was cultivar independent. In contrast, I. europaea had no visible effect on Populus growth. Metatranscriptomic studies reveal that these fungi impact rhizophytic and endophytic activities in Populus and induce shifts in soil and root microbial communities. Differential expression of core genes in P. trichocarpa roots was observed in response to both fungal species. Expression of Populus genes for lipid signaling and nutrient uptake were up-regulated and expression of genes associated with gibberellin signaling were altered in plants inoculated with M elongata, but not I. europaea. Up-regulation of genes for growth promotion, down-regulation of genes for several LRR-receptors/kinases, and alteration of expression of genes associated with plant defense responses (e.g., JA/ET/SA pathways) also suggest that M. elongata manipulates plant defenses while promoting plant growth.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

IMG/PR: a database of plasmids from genomes and metagenomes with rich annotations and metadata

Plasmids are mobile genetic elements found in many clades of Archaea and Bacteria. They drive horizontal gene transfer, impacting ecological and evolutionary processes within microbial communities, and hold substantial importance in human health and biotechnology. To support plasmid research and provide scientists with data of an unprecedented diversity of plasmid sequences, we introduce the IMG/PR database, a new resource encompassing 699 973 plasmid sequences derived from genomes, metagenomes and metatranscriptomes. IMG/PR is the first database to provide data of plasmid that were systematically identified from diverse microbiome samples. IMG/PR plasmids are associated with rich metadata that includes geographical and ecosystem information, host taxonomy, similarity to other plasmids, functional annotation, presence of genes involved in conjugation and antibiotic resistance. The database offers diverse methods for exploring its extensive plasmid collection, enabling users to navigate plasmids through metadata-centric queries, plasmid comparisons and BLAST searches. The web interface for IMG/PR is accessible at https://img.jgi.doe.gov/pr. Plasmid metadata and sequences can be downloaded from https://genome.jgi.doe.gov/portal/IMG_PR.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

WHONDRS-GUI: a web application for global survey of surface water metabolites

Background The Worldwide Hydrobiogeochemistry Observation Network for Dynamic River Systems (WHONDRS) is a consortium that aims to understand complex hydrologic, biogeochemical, and microbial connections within river corridors experiencing perturbations such as dam operations, floods, and droughts. For one ongoing WHONDRS sampling campaign, surface water metabolite and microbiome samples are collected through a global survey to generate knowledge across diverse river corridors. Metabolomics analysis and a suite of geochemical analyses have been performed for collected samples through the Environmental Molecular Sciences Laboratory (EMSL). The obtained knowledge and data package inform mechanistic and data-driven models to enhance predictions of outcomes of hydrologic perturbations and watershed function, one of the most critical components in model-data integration. To support efforts of the multi-domain integration and make the ever-growing data package more accessible for researchers across the world, a Shiny/R Graphical User Interface (GUI) called WHONDRS-GUI was created. Results The web application can be run on any modern web browser without any programming or operational system requirements, thus providing an open, well-structured, discoverable dataset for WHONDRS. Together with a context-aware dynamic user interface, the WHONDRS-GUI has functionality for searching, compiling, integrating, visualizing and exporting different data types that can easily be used by the community. The web application and data package are available at https://data.ess-dive.lbl.gov/view/doi:10.15485/1484811 , which enables users to simultaneously obtain access to the data and code and to subsequently run the web app locally. The WHONDRS-GUI is also available for online use at Shiny Server ( https://xmlin.shinyapps.io/whondrs/ ).

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2018

Mercury in Water

Mercury (Hg) is a global pollutant threatening our water resources and human health. Every one of us contains some levels of Hg or methylmercury (MeHg) in our body due to consumption of contaminated food such as fish and rice. Our understanding of the behavior of Hg in natural aquatic environments is limited as the major factors controlling microbial uptake and conversion of inorganic Hg to neurotoxic MeHg remain obscure. MeHg concentrations in water can bioaccumulate up to eight orders of magnitude in the food chain. Metallic or elemental Hg can evaporate and transport around the globe, and also readily undergoes chemical, photochemical and biological transformations (i.e., oxidation, reduction, methylation and demethylation) in water and sediments. Natural dissolved organic matter (DOM) plays a critical role in mediating these transformations because of its exceptionally strong binding affinity for Hg and its dual functional roles in reducing and oxidizing Hg. While the discovery of Hg-methylation genes significantly advanced our understanding of MeHg biosynthesis, the simultaneous degradation of MeHg at low concentrations (i.e., picomolar to nanomolar) by a range of methanotrophic and anaerobic bacteria has recently been recognized possibly as an important process for controlling net MeHg production, a key factor that determines Hg concentrations and bioaccumulation in biota. Although treatment technologies for Hg removal from water are available, they are mostly applicable to industrial waste streams and at localized contamination sites with high Hg concentrations (i.e., micromolar to millimolar). Reductions in Hg human exposure may be achievable by decreasing anthropogenic releases, such as coal combustion, over the long-term since Hg methylation responds to Hg inputs, particularly freshly deposited Hg in natural aquatic systems.

Gu, Baohua↗

DOE OSTI2022

Application of the metabolic modeling pipeline in KBase to categorize reactions, predict essential genes, and predict pathways in an isolate genome

The DOE Systems Biology Knowledgebase (KBase) platform offers a range of powerful tools for the reconstruction, refinement, and analysis of genome-scale metabolic models built from microbial isolate genomes. In this chapter, we describe and demonstrate these tools in action with an analysis of isoprene production in the Bacillus subtilis DSM genome. Two different methods are applied to build initial metabolic models for the DSM genome, then the models are gapfilled in three different growth conditions. Next, flux balance analysis (FBA) and flux variability analysis (FVA) techniques are applied to both study the growth of these models in minimal media and classify reactions within each model based on essentiality and functionality. The models are applied with the FBA method to predict essential genes, which are then compared to an updated list of essential genes obtained for B. subtilis 168, a very similar strain to the DSM isolate. The models are also applied to simulate Biolog growth conditions, and these results are compared with Biolog data collected for B. subtilis 168. Finally, the DSM metabolic models are applied to explore the pathways and genes responsible for producing isoprene in this strain. These studies demonstrate the accuracy and utility of models generated from the KBase pipelines, as well as exploring the tools available for analyzing these models.

DOE knowledgebase↗

DOE OSTI2023

Reverse engineering environmental metatranscriptomes clarifies best practices for eukaryotic assembly

Abstract Background Diverse communities of microbial eukaryotes in the global ocean provide a variety of essential ecosystem services, from primary production and carbon flow through trophic transfer to cooperation via symbioses. Increasingly, these communities are being understood through the lens of omics tools, which enable high-throughput processing of diverse communities. Metatranscriptomics offers an understanding of near real-time gene expression in microbial eukaryotic communities, providing a window into community metabolic activity. Results Here we present a workflow for eukaryotic metatranscriptome assembly, and validate the ability of the pipeline to recapitulate real and manufactured eukaryotic community-level expression data. We also include an open-source tool for simulating environmental metatranscriptomes for testing and validation purposes. We reanalyze previously published metatranscriptomic datasets using our metatranscriptome analysis approach. Conclusion We determined that a multi-assembler approach improves eukaryotic metatranscriptome assembly based on recapitulated taxonomic and functional annotations from an in-silico mock community. The systematic validation of metatranscriptome assembly and annotation methods provided here is a necessary step to assess the fidelity of our community composition measurements and functional content assignments from eukaryotic metatranscriptomes.

Krinos, Arianna I. (ORCID:0000000197678392)↗

DOE OSTI2021

Application of the Metabolic Modeling Pipeline in KBase to Categorize Reactions, Predict Essential Genes, and Predict Pathways in an Isolate Genome

Allen, Benjamin↗

DOE OSTI2018

Model‐Based Analysis of the Effects of Dam‐Induced River Water and Groundwater Interactions on Hydro‐Biogeochemical Transformation of Redox Sensitive Contaminants in a Hyporheic Zone

Abstract Biogeochemical processes in the hyporheic zone (HZ) may retard the contaminants migration from groundwater to the river and vice versa. Anthropogenic activities may further complicate such processes. This study investigated the effects of dam‐induced hydrodynamics on biogeochemical transformation of contaminants using Cr as an example in the HZ of the Columbia River at the U.S. Department of Energy's Hanford Site. The flow velocities in the HZ were first simulated using the measured or averaged groundwater level and river stage at hourly, daily, weekly, and monthly time scales. The flow velocities were then incorporated into a reactive transport model with independently characterized biogeochemical reactions and kinetics. Simulation results indicated that hydrodynamics can significantly influence the rate and extent of Cr (VI) biogeochemical transformation, which was mainly controlled by the kinetic reduction of Cr (VI) to sparely soluble Cr (III) by sediment‐associated Fe (II) that can be regenerated by microorganisms with organic carbon as electron donor. The frequent flow direction reversals in the HZ induced by dam operations enhanced the rate of microbial consumption of bioavailable OC, which, if there was no organic carbon supply, can eventually terminate the Fe (II) regeneration mechanism and exhaust the HZ's redox capacity in reducing Cr (VI) to Cr (III). This study demonstrated the importance of hydrodynamics on biogeochemical transformation of contaminants in the HZ and of the time scales used in assessing the reactive transport of chemicals and contaminants in the HZ as the net supply of redox sensitive chemicals such as dissolved oxygen into the HZ is a function of the frequency of flow direction reversal.

Yang, Chen↗

DOE OSTI2019

Investigating the Effect of Sorbed Humic Acid on the Mobility of Uranium - 19461

The Savannah River Site (SRS) was one of the major nuclear facilities for the U.S Department of Energy. During the Cold War, these facilities produced large amounts of radioactive and hazardous waste. On site, the F-Area consisted of three unlined seepage basins that collected approximately 6.8 billion liters of low-level waste that contained nitric acid, radionuclides, and dissolved metals due to plutonium separation operations. Sufficient quantities of uranium isotopes, I-129, Tc-99, and tritium migrated into the groundwater, creating an acidic plume with a pH between 3 and 5.5. Although the basins functioned as designed, the acidic nature of the waste created a source of contamination for the groundwater and soil below the basins. With radionuclides above their maximum contaminant level (MCL) remediation efforts took place. Humic acid as a remediation technology has shown potential for controlling radionuclide mobility. Humic acid is a fraction of humic substance that are ubiquitous in the environment. Humic substances (HS) are complex heterogeneous mixtures of polydispersed materials formed by biochemical and chemical reactions during the decay and transformation of plant and microbial remains. Humic substances account for 50-80% of the organic carbon in the soil or sediment and are known for their excellent binding capacity for metals. Humic acid can be extracted with a potassium hydroxide base solution and then drying it. The high pH solubilizes the humic acid molecules and generates a dark-brown highly-concentrated solution, rich in humic acid, which can be diluted for use. Humic acid's strong sorption capacity and its ability to develop a bond with uranium at slightly acid pH constitute it as remediation technology to reduce uranium (VI) mobility. Column experiments were performed to identify the sorption and desorption of HS in flow-through porous media representative of the acidic aquifer at the F-Area Seepage Basins. Two commercially available HA were selected for comparison, Huma-K and KW15 modified humics (modified humic acid, mod-HA). By conducting a nonreactive rhenium tracer test, on columns filled with soil obtained from SRS's FAW-1 at a depth interval of 18 m -21 m, column parameters such as pore volume (PV), variance, dispersion and peclet number were determined. Columns were then used to estimate the influence of HA on uranium mobility. Data obtained from this study shows that using HA as an amendment for uranium remediation improves uranium removal significantly. (authors)

12 MANAGEMENT OF RADIOACTIVE AND NON-RADIOACTIVE W↗

DOE OSTI2021

Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes

Abstract The herbivore digestive tract is home to a complex community of anaerobic microbes that work together to break down lignocellulose. These microbiota are an untapped resource of strains, pathways and enzymes that could be applied to convert plant waste into sugar substrates for green biotechnology. We carried out more than 400 parallel enrichment experiments from goat faeces to determine how substrate and antibiotic selection influence membership, activity, stability and chemical productivity of herbivore gut communities. We assembled 719 high-quality metagenome-assembled genomes (MAGs) that are unique at the species level. More than 90% of these MAGs are from previously unidentified herbivore gut microorganisms. Microbial consortia dominated by anaerobic fungi outperformed bacterially dominated consortia in terms of both methane production and extent of cellulose degradation, which indicates that fungi have an important role in methane release. Metabolic pathway reconstructions from MAGs of 737 bacteria, archaea and fungi suggest that cross-domain partnerships between fungi and methanogens enabled production of acetate, formate and methane, whereas bacterially dominated consortia mainly produced short-chain fatty acids, including propionate and butyrate. Analyses of carbohydrate-active enzyme domains present in each anaerobic consortium suggest that anaerobic bacteria and fungi employ mostly complementary hydrolytic strategies. The division of labour among herbivore anaerobes to degrade plant biomass could be harnessed for industrial bioprocessing.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Prokaryotic viruses impact functional microorganisms in nutrient removal and carbon cycle in wastewater treatment plants

As one of the largest biotechnological applications, activated sludge (AS) systems in wastewater treatment plants (WWTPs) harbor enormous viruses, with 10-1,000-fold higher concentrations than in natural environments. However, the compositional variation and host-connections of AS viruses remain poorly explored. Here, we report a catalogue of ~50,000 prokaryotic viruses from six WWTPs, increasing the number of described viral species of AS by 23-fold, and showing the very high viral diversity which is largely unknown (98.4-99.6% of total viral contigs). Most viral genera are represented in more than one AS system with 53 identified across all. Viral infection widely spans 8 archaeal and 58 bacterial phyla, linking viruses with aerobic/anaerobic heterotrophs, and other functional microorganisms controlling nitrogen/phosphorous removal. Notably, Mycobacterium, notorious for causing AS foaming, is associated with 402 viral genera. Our findings expand the current AS virus catalogue and provide reference for the phage treatment to control undesired microorganisms in WWTPs.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2018

Structural insights into inhibitor binding to a fungal ortholog of aspartate semialdehyde dehydrogenase

Highlights: • Structure of an inhibitor bound to an essential fungal enzyme. • Effects of cofactor binding on oligomeric assembly. • Structure guided docking of a potent fungal enzyme inhibitor. • Structural comparison to related microbial enzymes. The aspartate pathway, uniquely found in plants and microorganisms, offers novel potential targets for the development of new antimicrobial drugs. Aspartate semialdehyde dehydrogenase (ASADH) catalyzes production of a key intermediate at the first branch point in this pathway. Several fungal ASADH structures have been determined, but the prior crystallization conditions had precluded complex formation with enzyme inhibitors. The first inhibitor-bound and cofactor-bound structures of ASADH from the pathogenic fungi Blastomyces dermatitidis have now been determined, along with a structural and functional comparison to other ASADH family members. The structure of this new ASADH is similar to the other fungal orthologs, but with some critical differences in the orientation of some active site functional groups and in the subunit interface region. The presence of this bound inhibitor reveals the first details about inhibitor binding interactions, and the flexible orientation of its aromatic ring provides helpful insights into the design of potentially more potent and selective antifungal compounds.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2023

Continuous multimodal technologies in industrial microbiology: potential for achieving high process performance and agility

The field of industrial microbiology has great potential to tackle the most pressing challenges facing society, but today, this entails much more than classical fermentation technology followed by product upgrading. Methods are needed to confer unit-operation-level functionality and whole-system-level robustness, as well as flexibility. As examples of this concept, we focus here on methodologies often deployed at industrial scale as discrete processes—such as biological, chemical, and electrochemical unit operations—that are also capable of substantial complementarity when combined sequentially and operated continuously. A key and relatively new type of conversion step is made possible by catalyst immobilization methods at both the enzymatic and cellular level. Cases drawn from electro-fermentation for acetoin production and syngas-mediated microbial electrosynthesis of ethanol exemplify the synergy of combined operational approaches. Because modular processes can be treated as a series of reactor elements, considerable flexibility is possible. As discussed, however, not all processes are amenable to this intensification.

09 BIOMASS FUELS↗

DOE OSTI2024

Cyanobacteria from marine oxygen-deficient zones encode both form I and form II Rubiscos

Cyanobacteria are highly abundant in the marine photic zone and primary drivers of the conversion of inorganic carbon into biomass. To date, all studied cyanobacterial lineages encode carbon fixation machinery relying upon form I Rubiscos within a CO 2 -concentrating carboxysome. Here, we report that the uncultivated anoxic marine zone (AMZ) IB lineage ofProchlorococcusfrom pelagic oxygen-deficient zones (ODZs) harbors both form I and form II Rubiscos, the latter of which are typically noncarboxysomal and possess biochemical properties tuned toward low-oxygen environments. We demonstrate that these cyanobacterial form II enzymes are functional in vitro and were likely acquired from proteobacteria. Metagenomic analysis reveals that AMZ IB are essentially restricted to ODZs in the Eastern Pacific, suggesting that form II acquisition may confer an advantage under low-O 2 conditions. AMZ IB populations express both forms of Rubisco in situ, with the highest form II expression at depths where oxygen and light are low, possibly as a mechanism to increase the efficiency of photoautotrophy under energy limitation. Our findings expand the diversity of carbon fixation configurations in the microbial world and may have implications for carbon sequestration in natural and engineered systems.

Science & Technology - Other Topics↗

DOE OSTI2022

Quantifying the inhibitory impact of soluble phenolics on anaerobic carbon mineralization in a thawing permafrost peatland

The mechanisms controlling the extraordinarily slow carbon (C) mineralization rates characteristic of Sphagnum -rich peatlands (“bogs”) are not fully understood, despite decades of research on this topic. Soluble phenolic compounds have been invoked as potentially significant contributors to bog peat recalcitrance due to their affinity to slow microbial metabolism and cell growth. Despite this potentially significant role, the effects of soluble phenolic compounds on bog peat C mineralization remain unclear. We analyzed this effect by manipulating the concentration of free soluble phenolics in anaerobic bog and fen peat incubations using water-soluble polyvinylpyrrolidone (“PVP”), a compound that binds with and inactivates phenolics, preventing phenolic-enzyme interactions. CO 2 and CH 4 production rates (end-products of anaerobic C mineralization) generally correlated positively with PVP concentration following Michaelis-Menten (M.M.) saturation functions. Using M.M. parameters, we estimated that the extent to which phenolics inhibit anaerobic CO 2 production was significantly higher in the bog—62 ± 16%—than the fen—14 ± 4%. This difference was found to be more substantial with regards to methane production—wherein phenolic inhibition for the bog was estimated at 54 ± 19%, while the fen demonstrated no apparent inhibition. Consistent with this habitat difference, we observed significantly higher soluble phenolic content in bog vs. fen pore-water. Together, these findings suggest that soluble phenolics could contribute to bogs’ extraordinary recalcitrance and high (relative to other peatland habitats) CO 2 :CH 4 production ratios.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Stability Analysis of Parameter Varying Genetic Toggle Switches Using Koopman Operators

The genetic toggle switch is a well known model in synthetic biology that represents the dynamic interactions between two genes that repress each other. The mathematical models for the genetic toggle switch that currently exist have been useful in describing circuit dynamics in rapidly dividing cells, assuming fixed or time-invariant kinetic rates. There is a growing interest in being able to model and extend synthetic biological function for growth conditions such as stationary phase or during nutrient starvation. As cells transition from one growth phase to another, kinetic rates become time-varying parameters. In this paper, we propose a novel class of parameter varying nonlinear models that can be used to describe the dynamics of genetic circuits, including the toggle switch, as they transition from different phases of growth. We show that there exists unique solutions for this class of systems, as well as for a class of systems that incorporates the microbial phenomena of quorum sensing. Further, we show that the domain of these systems, which is the positive orthant, is positively invariant. We also showcase a theoretical control strategy for these systems that would grant asymptotic monostability of a desired fixed point. We then take the general form of these systems and analyze their stability properties through the framework of time-varying Koopman operator theory. A necessary condition for asymptotic stability is also provided as well as a sufficient condition for instability. A Koopman control strategy for the system is also proposed, as well as an analogous discrete time-varying Koopman framework for applications with regularly sampled measurements.

Harrison, Jamiree (ORCID:0000000265351579)↗

DOE OSTI2025

Beneath the surface: Unsolved questions in soil virus ecology

Soil virus ecology is an exciting but still nascent field of research in soil microbiology. While there has been a recent surge in soil virus research studies, many fundamental questions remain unanswered, and a range of technical and bioinformatic challenges need to be overcome. In this perspective article, we present a series of key questions that highlight fruitful research areas for ongoing and future efforts. These include describing the challenges involved in understanding soil viral abundance and activity, spatiotemporal dynamics, life strategy prevalence, virus-mediated biogeochemical impacts, viral protein function, host prediction, and soil RNA virus discovery. In the near term, combining approaches (e.g., cultivation-based, meta-omics, biogeochemical, experimental, and bioinformatic) will be key to assessing the ecological and biogeochemical impacts of soil viruses from the microscopic to the field and global scales. Still, we stress that results must be tempered by current methodological limitations and highlight knowledge gaps that are most pressing to fill via new methods or measurements, such as the prevalence of different viral replication strategies across soils, the fate of microbial necromass carbon after viral lysis, the frequency of virus-host encounters that do not lead to successful infections yet could be bioinformatically mistaken as infections, and the diversity and ecological impacts of RNA viruses in soil.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Phylogenetic and ecological drivers of the avian lung mycobiome and its potentially pathogenic component

Vertebrate lungs contain diverse microbial communities, but little is known about the drivers of community composition or consequences for health. Microbiome assembly by processes such as dispersal, coevolution, and host-switching can be probed with comparative surveys; however, few studies exist for lung microbiomes, particularly for the fungal component, the mycobiome. Distinguishing among fungal taxa that are generalist or specialist symbionts, potential pathogens, or incidentally inhaled spores is urgent because of potential for emerging diseases. Here, we characterize the avian lung mycobiome and test the relative influences of environment, phylogeny, and functional traits. We used metabarcoding and culturing from 195 lung samples representing 32 bird species across 20 families. We identified 526 fungal taxa as estimated by distinct sequence types (zOTUs) including many opportunistic pathogens. These were predominantly from the phylum Ascomycota (79%) followed by Basidiomycota (16%) and Mucoromycota (5%). Yeast and yeast-like taxa (Malassezia, Filobasidium, Saccharomyces, Meyerozyma, and Aureobasidium) and filamentous fungi (Cladosporium, Alternaria, Neurospora, Fusarium, and Aspergillus) were abundant. Lung mycobiomes were strongly shaped by environmental exposure, and further modulated by host identity, traits, and phylogenetic affinities. Our results implicate migratory bird species as potential vectors for long-distance dispersal of opportunistically pathogenic fungi.

59 BASIC BIOLOGICAL SCIENCES↗