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DOE OSTI2021

Genome Extraction from Shotgun Metagenome Sequence Data

Uncultivated Bacteria and Archaea comprise the vast majority of species on Earth, but obtaining their genomes directly from the environment, using shotgun sequencing, has only recently become possible. To realize the hope of capturing Earth’s microbial genetic complement, technologies that accelerate recovery of high-quality genomes are necessary. We present a series of analysis steps and data products for the extraction of high quality metagenome-assembled genomes (MAGs) from microbiomes using the U.S. Department of Energy Systems Biology Knowledgebase (KBase) platform (http://www.kbase.us/). In KBase, the process is end-to-end, allowing a user to go from the initial sequencing reads all the way through to MAG genomes, which can then be analyzed with other KBase capabilities such as phylogenetic placement, functional assignment, metabolic modeling, pangenome functional profiling, RNA-Seq, and others. While portions of such capabilities are individually available from other resources, the combination of the intuitive usability, data interoperability, and integration of tools in a freely available compute resource makes KBase a uniquely powerful platform for obtaining MAGs from microbiomes. While this workflow offers tools for each of the key steps in the genome extraction process, it also provides a scaffold that can be easily extended, with additional MAG recovery and analysis tools, via the KBase SDK (Software Development Kit).

Chivian, Dylan↗

DOE OSTI2021

Moab Desert Crust - Sample 4E

Chivian, Dylan↗

DOE OSTI2023

Editorial for Special Issue “Advances in Soil Microbiome”

The soil microbiome (the community of all soil microorganisms and their surrounding environment) is a critical part of our ecological network. These microbial communities carry out several important functions, including the promotion of plant growth and the cycling of carbon and nitrogen sources. Despite the importance of this community, and the recent advances in multi-omic analysis and other methods designed to query complex systems, there is a still a large knowledge gap regarding the soil microbiome, its response to changing climates and moisture levels, the specific molecular mechanisms that drive its role in the environment, and how these questions can be answered through the use of model systems. Here, we present eleven new papers that seek to answer these questions and expand our knowledge of the soil microbiome.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS1977

The effect of 1 to 5 keV electrons on the reproductive integrity of microorganisms

Microorganisms were exposed to simulated space environment in order to assess the effect of electrons in the energy range 1 to 5 keV on their colony-forming ability. The test system consisted of an electron gun and power supply, a dosimetry subsystem, and a vacuum subsystem. The system was capable of current densities ranging from 0.1 nA/sq cm to 5 micro A/sq cm on a 25 sq on target and an ultimate vacuum of 0.0006 N/sq m (0.000004 torr). The results of the experimental program show a significant reduction in microbial reproductive integrity.

Barengoltz, J. B.↗

NASA NTRS2015

Veggie ISS Validation Test Results and Produce Consumption

The Veggie vegetable production system flew to the International Space Station (ISS) in the spring of 2014. The first set of plants, Outredgeous red romaine lettuce, was grown, harvested, frozen, and returned to Earth in October. Ground control and flight plant tissue was sub-sectioned for microbial analysis, anthocyanin antioxidant phenolic analysis, and elemental analysis. Microbial analysis was also performed on samples swabbed on orbit from plants, Veggie bellows, and plant pillow surfaces, on water samples, and on samples of roots, media, and wick material from two returned plant pillows. Microbial levels of plants were comparable to ground controls, with some differences in community composition. The range in aerobic bacterial plate counts between individual plants was much greater in the ground controls than in flight plants. No pathogens were found. Anthocyanin concentrations were the same between ground and flight plants, while antioxidant and phenolic levels were slightly higher in flight plants. Elements varied, but key target elements for astronaut nutrition were similar between ground and flight plants. Aerobic plate counts of the flight plant pillow components were significantly higher than ground controls. Surface swab samples showed low microbial counts, with most below detection limits. Flight plant microbial levels were less than bacterial guidelines set for non-thermostabalized food and near or below those for fungi. These guidelines are not for fresh produce but are the closest approximate standards. Forward work includes the development of standards for space-grown produce. A produce consumption strategy for Veggie on ISS includes pre-flight assessments of all crops to down select candidates, wiping flight-grown plants with sanitizing food wipes, and regular Veggie hardware cleaning and microbial monitoring. Produce then could be consumed by astronauts, however some plant material would be reserved and returned for analysis. Implementation of this plan is a step toward developing pick-and-eat food production to supplement the packaged diet on ISS and for future exploration missions where plants could make up a larger portion of the diet. Supported by NASA Space Biology Program.

Food Safety↗

NASA NTRS2016

Effects of Material Choice on Biocide Loss in Orion Water Storage Tanks

When preparing for long-duration spaceflight missions, maintaining a safe supply of potable water is of the utmost importance. One major aspect of that is ensuring that microbial growth is minimized. Historically, this challenge has been addressed through the use of biocides. When using biocides, the choice of materials for the storage containers is important, because surface reactions can reduce biocide concentrations below their effective range. In the water storage system baselined for the Orion vehicle, the primary wetted materials are stainless steel (316 L) and a titanium alloy (Ti6Al4V). Previous testing with these materials has shown that the biocide selected for use in the system (ionic silver) will plate out rapidly upon initial wetting of the system. One potential approach for maintaining an adequate biocide concentration is to spike the water supply with high levels of biocide in an attempt to passivate the surface. To evaluate this hypothesis, samples of the wetted materials were tested individually and together to determine the relative loss of biocide under representative surface area-to-volume ratios after 24 hours. Additionally, we have analyzed the efficacy of disinfecting a system containing these materials by measuring reductions in bacterial counts in the same test conditions. Preliminary results indicate that the use of titanium, either individually or in combination with stainless steel, can result in over 95% loss of biocide, while less than 5% is lost when using stainless steel. In bacterial testing, viable organisms were recovered from samples exposed to the titanium coupons after 24 hours. By comparison, no organisms were recovered from the test vessels containing only stainless steel. These results indicate that titanium, while possessing some favorable attributes, may pose additional challenges when used in water storage tanks with ionic silver biocide.

Wallace, W. T.↗

NASA NTRSDate not supplied

Decadal Changes in Barrier Island Facies near Mansfield Pass on Padre Island, Texas from 1950-Present

Barrier islands serve an important role in shielding coastal areas from storms and wave erosion. Monitoring changes in barrier island systems helps understand the effect of storms and sea level rise on the stability of the island. The study area is at Padre Island, near Mansfield Pass, has seen wide-spread changes in surface morphology underpinned by significant growth of vegetation and microbial mats.

Kenton R. Fisher↗

DOE OSTI2026

From viruses to protists: temperature response of the neglected components of microbial controls on peatland nutrient cycling

The response of plant-associated microbial communities to rising temperatures likely plays a key role in global Carbon (C) and Nitrogen (N) biogeochemical cycles. Mosses of the genus Sphagnum, in particular, sequester 25% of all terrestrial C as recalcitrant peat. However, their ability to sequester C is mediated by interactions with microbes that fix N and pass it to the moss to grow in otherwise oligotrophic systems. Two important biotic controls on this processes are likely to respond to rising temperatures –predation by protists and infections by viruses– but whether and how this might occur is not well understood. This proposal addressed these questions using a combination of genomics and mathematical modeling with both field data from whole-ecosystem warming experiments, and laboratory-based microcosm experiments. We have discovered 1) mechanistic links between cell traits and thermal performance in protists, which 2) enabled predictions from populations to ecosystems, 3) we have identified eco-phenotypic feedbacks that determine protist–bacterial predator–prey dynamics, 4) have documented concomitant compositional and trait shifts in protist communities with warming in the field, 5) revealed consistent interactive effects of temperature and nutrients on bacterial and protist communities; 6) characterized the Sphagnum virome, and 7) made modeling predictions on its implications for thermal responses of microbial communities in peatlands globally. This award also substantially strengthened U.S. scientific capacity and workforce development.

Gibert, Jean Philippe [Duke University]↗

NASA NTRS2002

Spatial distribution of total, ammonia-oxidizing, and denitrifying bacteria in biological wastewater treatment reactors for bioregenerative life support

Bioregenerative life support systems may be necessary for long-term space missions due to the high cost of lifting supplies and equipment into orbit. In this study, we investigated two biological wastewater treatment reactors designed to recover potable water for a spacefaring crew being tested at Johnson Space Center. The experiment (Lunar-Mars Life Support Test Project-Phase III) consisted of four crew members confined in a test chamber for 91 days. In order to recycle all water during the experiment, an immobilized cell bioreactor (ICB) was employed for organic carbon removal and a trickling filter bioreactor (TFB) was utilized for ammonia removal, followed by physical-chemical treatment. In this study, the spatial distribution of various microorganisms within each bioreactor was analyzed by using biofilm samples taken from four locations in the ICB and three locations in the TFB. Three target genes were used for characterization of bacteria: the 16S rRNA gene for the total bacterial community, the ammonia monooxygenase (amoA) gene for ammonia-oxidizing bacteria, and the nitrous oxide reductase (nosZ) gene for denitrifying bacteria. A combination of terminal restriction fragment length polymorphism (T-RFLP), sequence, and phylogenetic analyses indicated that the microbial community composition in the ICB and the TFB consisted mainly of Proteobacteria, low-G+C gram-positive bacteria, and a Cytophaga-Flexibacter-Bacteroides group. Fifty-seven novel 16S rRNA genes, 8 novel amoA genes, and 12 new nosZ genes were identified in this study. Temporal shifts in the species composition of total bacteria in both the ICB and the TFB and ammonia-oxidizing and denitrifying bacteria in the TFB were also detected when the biofilms were compared with the inocula after 91 days. This result suggests that specific microbial populations were either brought in by the crew or enriched in the reactors during the course of operation.

NASA Discipline Life Support Systems↗

DOE OSTI2023

Deep anoxic aquifers could act as sinks for uranium through microbial-assisted mineral trapping

Uptake of uranium (U) by secondary minerals, such as carbonates and iron (Fe)-sulfides, that occur ubiquitously on Earth, may be substantial in deep anoxic environments compared to surficial settings due to different environment-specific conditions. Yet, knowledge of U reductive removal pathways and related fractionation between 238 U and 235 U isotopes in deep anoxic groundwater systems remain elusive. Here we show bacteria-driven degradation of organic constituents that influences formation of sulfidic species facilitating reduction of geochemically mobile U(VI) with subsequent trapping of U(IV) by calcite and Fe-sulfides. The isotopic signatures recorded for U and Ca in fracture water and calcite samples provide additional insights on U(VI) reduction behaviour and calcite growth rate. The removal efficiency of U from groundwater reaching 75% in borehole sections in fractured granite, and selective U accumulation in secondary minerals in exceedingly U-deficient groundwater shows the potential of these widespread mineralogical sinks for U in deep anoxic environments.

36 MATERIALS SCIENCE↗

DOE OSTI2020

Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

Little is known about viruses in oxygen-deficient water columns (ODWCs). In surface ocean waters, viruses are known to act as gene vectors among susceptible hosts. Some of these genes may have metabolic functions and are thus termed auxiliary metabolic genes (AMGs). AMGs introduced to new hosts by viruses can enhance viral replication and/or potentially affect biogeochemical cycles by modulating key microbial pathways. Here we identify 748 viral populations that cluster into 94 genera along a vertical geochemical gradient in the Cariaco Basin, a permanently stratified and euxinic ocean basin. The viral communities in this ODWC appear to be relatively novel as 80 of these viral genera contained no reference viral sequences, likely due to the isolation and unique features of this system. We identify viral elements that encode AMGs implicated in distinctive processes, such as sulfur cycling, acetate fermentation, signal transduction, [Fe–S] formation, and N-glycosylation. These AMG-encoding viruses include two putative Mu-like viruses, and viral-like regions that may constitute degraded prophages that have been modified by transposable elements. Our results provide an insight into the ecological and biogeochemical impact of viruses oxygen-depleted and euxinic habitats.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2013

The Sample Handling System for the Mars Icebreaker Life Mission: from Dirt to Data

The Mars icebreaker life mission will search for subsurface life on mars. It consists of three payload elements: a drill to retrieve soil samples from approx. 1 meter below the surface, a robotic sample handling system to deliver the sample from the drill to the instruments, and the instruments themselves. This paper will discuss the robotic sample handling system.

Martian Arctic↗

DOE OSTI2024

Getting to the root of the problem: Soil carbon and microbial responses to root inputs within a buried paleosol along an eroding hillslope in southwestern Nebraska, USA

Large quantities of soil carbon (C) can persist within paleosols for millennia due to burial and subsequent isolation from plant-derived inputs, atmospheric conditions, and microbial activity at the modern surface. Erosion exposes buried soils to modern root-derived C influx via root exudation and root turnover, thus stimulating microbial activity leading to SOC decomposition and accumulation through organo-mineral stabilization of modern C. With this study we aim to quantify how modern root-derived C inputs impact paleosol C decomposition and stabilization across varying degrees of isolation from modern surface conditions in southwestern Nebraska, USA, where hillslope erosion is bringing a buried Late-Pleistocene-early Holocene paleosol (the “Brady Soil”) closer to the modern surface. We collected Brady Soil samples from 0.2m, 0.4m, and 1.2m below the modern surface and conducted two lab-based incubations. Soils were amended with either (1) a lab-synthesized mixture of low molecular weight compounds (12 atom% 13 C), or (2) 13 C enriched root residues (92 atom% 13 C), in 30-day and 240-day incubation experiments, respectively. Here we determined microbial responses to synthetic root exudates and residues by partitioning the 13 C label from Brady Soil C, including measurements of total, root, and primed C respiration, microbial biomass C (MBC), microbial C use efficiency (CUE). To assess the capacity of isolated paleosols to accrue modern plant C, we used Nano-scale Secondary Ion Mass Spectrometry imaging. We found that: (1) adding root-derived C inputs primed Brady Soil C across all depths, and was mediated by depth and composition of root additions; (2) root-derived C inputs stimulated microbial biomass C (MBC) growth similarly across depths, but the magnitude of CUE and MBC varied by chemistry of root-derived additions; (3) new particulate organic matter was incorporated into mineral-associated pools over time; (4) material from the added root residues was found in association with bacterial cells and fungal hyphae as well as with soil aggregate and mineral surfaces. Our study shows that paleosols defy expectations of C content and reactivity with depth, and changes in land cover and climate will expose buried paleosols to modern surface conditions, increasing respired C. This work highlights the importance of evaluating the role resurfacing buried soils through landscape change plays in C cycle feedbacks to the climate system.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2023

Determining the biogeochemical transformations of organic matter composition in rivers using molecular signatures

Inland waters are hotspots for biogeochemical activity, but the environmental and biological factors that govern the transformation of organic matter (OM) flowing through them are still poorly constrained. Here we evaluate data from a crowdsourced sampling campaign led by the Worldwide Hydrobiogeochemistry Observation Network for Dynamic River Systems (WHONDRS) consortium to investigate broad continental-scale trends in OM composition compared to localized events that influence biogeochemical transformations. Samples from two different OM compartments, sediments and surface water, were collected from 97 streams throughout the Northern Hemisphere and analyzed to identify differences in biogeochemical processes involved in OM transformations. By using dimensional reduction techniques, we identified that putative biogeochemical transformations and microbial respiration rates vary across sediment and surface water along river continua independent of latitude (18°N–68°N). In contrast, we reveal small- and large-scale patterns in OM composition related to local (sediment vs. water column) and reach (stream order, latitude) characteristics. These patterns lay the foundation to modeling the linkage between ecological processes and biogeochemical signals. We further showed how spatial, physical, and biogeochemical factors influence the reactivity of the two OM pools in local reaches yet find emergent broad-scale patterns between OM concentrations and stream order. OM processing will likely change as hydrologic flow regimes shift and vertical mixing occurs on different spatial and temporal scales. As our planet continues to warm and the timing and magnitude of surface and subsurface flows shift, understanding changes in OM cycling across hydrologic systems is critical, given the unknown broad-scale responses and consequences for riverine OM.

rivers↗

NASA NTRS2011

VEGGIE Pillow Testing: Microbial Analysis of Cut-and-Come-Again Species Testing

With NASA focused on researching and developing technology for deep space missions, the need for a reliable supplementary food source must also be considered. For the ISS, resupplying the food source is more practical and cost effect since the facility is in low Earth orbit. However, as NASA attempts to push the frontier in space, the costs and distance for resupply will surely increase. Plants would contribute to the proportion of food and reduce the dependency on food from Earth. In addition, plants would provide oxygen production, carbon dioxide removal, and psychological benefits. As a result, a vegetable production system, VEGGIE, was developed for NASA to produce salad crops with minimal resources and study the beneficial effects. The VEGGIE pillow is a single use bag for growing crops that is used with the VEGGIE hardware. The VEGGIE pillow was tested with four different species of plants with the cut-and-come-again harvest method to determine the greatest yield. Instead of harvesting the entire plant, the harvest consisted of cutting leaves to allow the plant to regrow leaves. The harvest methods included cutting the plants weekly, bi-weekly, and monthly. A fifth plant species, radishes, was also harvested and replanted. Microbial load analysis and an ANOVA significance test were utilized. The data suggest that the two Brassica plants have the greatest yields; however, the microbial load is also greatest for the two plants per gram of fresh weight. Furthermore, the results support the reuse of pillows for multiple harvests as shown by the replanted radishes.

Nguyen, Bao-Thang↗

DOE OSTI2024

How Does Escherichia coli Allocate Proteome?

Microorganisms are shown to actively partition their intracellular resources, such as pro- teins, for growth optimization. Recent experiments have begun to reveal molecular com- ponents unpinning the partition; however, it remains unclear quantitatively how individual parts orchestrate to yield precise resource allocation that is both robust and dynamic. Here we developed a coarse-grained mathematical framework that centers on guanosine pentaphosphate (ppGpp)-mediated regulation, and used it to systematically uncover the design principles of proteome allocation in Escherichia coli. Our results showed that cellular ability of resource partition lies in an ultrasensitive, negative feedback control- ling topology with the ultrasensitivity arising from zero-order amino acid kinetics and the negative feedback from ppGpp-controlled ribosome synthesis. In addition, together with the time-scale separation between slow ribosome kinetics and fast turnovers of ppGpp and amino acids, the network topology confers the organism an optimization mechanism which mimics sliding mode control, a nonlinear optimization strategy that is widely used in man-made systems. We further showed that such a controlling mechanism is robust against parameter variations and molecular fluctuations, and is also efficient for biomass production over time. Furthermore, this work elucidates the fundamental controlling mechanism of E. coli proteome allocation, thereby providing insights into quantitative microbial physiology as well as the design of synthetic gene networks.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Genetic Transfer in Action: Uncovering DNA Flow in an Extremophilic Microbial Community

ABSTRACT Horizontal genetic transfer (HGT) is a significant driver of genomic novelty in all domains of life. HGT has been investigated in many studies however, the focus has been on conspicuous protein‐coding DNA transfers that often prove to be adaptive in recipient organisms and are therefore fixed longer‐term in lineages. These results comprise a subclass of HGTs and do not represent exhaustive (coding and non‐coding) DNA transfer and its impact on ecology. Uncovering exhaustive HGT can provide key insights into the connectivity of genomes in communities and how these transfers may occur. In this study, we use the term frequency‐inverse document frequency (TF‐IDF) technique, that has been used successfully to mine DNA transfers within real and simulated high‐quality prokaryote genomes, to search for exhaustive HGTs within an extremophilic microbial community. We establish a pipeline for validating transfers identified using this approach. We find that most DNA transfers are within‐domain and involve non‐coding DNA. A relatively high proportion of the predicted protein‐coding HGTs appear to encode transposase activity, restriction‐modification system components, and biofilm formation functions. Our study demonstrates the utility of the TF‐IDF approach for HGT detection and provides insights into the mechanisms of recent DNA transfer.

Microbiology↗

DOE OSTI2023

A Systems Approach to Increasing Carbon Flux to Seed Oil for Biofuels and Bioproducts Production in Camelina sativa (Final Report)

To combat climate change and alleviate the dependency of the United States on fossil fuels, the transition to biofuel crops has long been proposed as a crucial part of the long-term solution. Camelina sativa has emerged as one of the leading commercially viable options for biofuel and bioproduct production for the U.S. Camelina has the advantages of low agronomic inputs and natural resistance to diverse biotic and abiotic stresses relative to other oilseed crops, and Camelina oil-based blends have been tested and approved as liquid transportation fuels. A major limitation in the widespread adoption of Camelina as a viable industrial oilseed crop is its modest oil yields. This project directly investigated possible paths towards increasing oil, by employing tissue-specific and whole plant systems approaches to identify major regulatory bottlenecks. We developed a new high-throughput method for the identification of multi-gene transformants in polyploid species like Camelina sativa and used this to determine that, contrary to what mathematical models suggested, introduction of the microbial Entner-Doudoroff (ED) pathway into Camelina sativa did not result in significant seed oil increases. We developed flux maps providing accurate and statistically robust models of central carbon metabolism in Camelina, including of cultured Camelina embryos. This knowledge was used in the capacitation of a number of junior researchers in gaining knowledge on approaches used for quantitative flux map analyses. We identified several novel Camelina transcription factor genes regulating fatty acid biosynthesis that showed variable effects on seed oil accumulation in transgenic plants. Among a number of community resources, we also developed a knowledge base web resource (CamRegBase) to integrate Camelina gene regulatory information. Together, research outcomes from this project have contributed to a much better understanding of the regulation and bottlenecks to engineer seed oil production in Camelina.

09 BIOMASS FUELS↗