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DOE OSTI2021

Engineering robust microorganisms for organic acid production

Abstract Organic acids are an important class of compounds that can be produced by microbial conversion of renewable feedstocks and have huge demands and broad applications in food, chemical, and pharmaceutical industries. An economically viable fermentation process for production of organic acids requires robust microbial cell factories with excellent tolerance to low pH conditions, high concentrations of organic acids, and lignocellulosic inhibitors. In this review, we summarize various strategies to engineer robust microorganisms for organic acid production and highlight their applications in a few recent examples.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Amplicon Sequencing Assessment to Measure Microbial Community Response from Heavy Metal Contaminated Soils in Savannah River site, Tims Branch watershed

Long-term presence of heavy metal contamination in soils is correlated with changes in microbial community structures and can lead to the reduction of indigenous species. Tolerance to soil heavy metal toxicity varies among different microbial communities. It remains unclear whether long term effects caused by metal perturbations are associated with soil microbial community dysregulation in Tims Branch watershed. Research Questions: Does heavy metal contamination in Tims Branch soils decrease microbial species diversity significantly compared to non-contaminated soils? Does the species richness decrease in contaminated samples? between samples? Is diversity in low, mid and high contamination soils significantly different compared to control samples? Hypothesis: The relative abundance and diversity of species are significantly altered in soils which are contaminated with heavy metals in the Tims Branch watershed. Objectives: Use amplicon sequencing technology along with bioinformatics to compare bacterial communities between four sites in Tims Branch watershed. Evaluate the percent relative abundance and diversity across the site. Conclusions: All bacterial communities exposed to different heavy metal concentrations were dominated by four major groups (Proteobacteria, Acidobacteria, Chloroflexi and Verrucomicrobia). The dominant phyla Proteobacteria, Acidobacteria and Chloroflexi accounted for 61 % of the relative abundance. Soil bacterial α-diversity, expressed as observed species richness metric and Shannon's diversity index, was the highest in sample location four (high contamination). The lowest observed was at the control location. Species richness increased when concentrations of heavy metals were localized, inferring that the metals can alter microbial community structure. PERMANOVA analysis between contaminated groups tested significant using the Adonis (F (4,29) =1.9712; p < 0.001). There is a 20 percent variation explained between groups (R2 = 0.214). This analysis proves to be beneficial in detecting microbial communities altered by contaminated soils. Moreover, certain concentrations of heavy metals can alter microbial community structures.

12 MANAGEMENT OF RADIOACTIVE AND NON-RADIOACTIVE W↗

DOE OSTI2023

Ecological strategies of microbes: Thinking outside the triangle

Abstract I asked whether Grime's triangle of competitive, stress tolerance and ruderal ecological strategies—which was originally developed for plants—applies to microbes. I conducted a synthesis of empirical studies that tested relationships among microbial traits presumed to define the competitive, stress tolerance and ruderal, and other ecological strategies. There was broad support for Grime's triangle. However, the ecological strategies were inconsistently linked to shifts in microbial communities under environmental changes like nitrogen and phosphorus addition, warming, drought, etc. We may be missing important ecological strategies that more closely influence microbial community composition under shifting environmental conditions. We may need to start by documenting changes in microbial communities in response to environmental conditions at fine spatiotemporal scales relevant for microbes. We can then develop empirically based ecological strategies, rather than modifying those based on plant ecology. Synthesis . Microbes appear to sort into similar ecological strategies as plants. However, these microbial ecological strategies do not consistently predict how community composition will shift under environmental change. By starting ‘from the ground up’, we may be able to delineate ecological strategies more relevant for microbes.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2026

Bio-based oxalic acid production in Issatchenkia orientalis enables sustainable rare earth recovery

The growing demand for rare earth elements (REEs) in clean energy and high-tech industries underscores the need for sustainable recovery methods and a reliable supply of processing chemicals. Here, we establish a microbial platform using the acid-tolerant yeast Issatchenkia orientalis SD108 to produce bio-oxalic acid for REE recovery. By introducing an oxaloacetate cleavage pathway and applying metabolic engineering, the engineered strain produces 39.53 g·L -1 oxalic acid at pH 4.0 in fed-batch fermentation. The crude fermentation broth, used without purification, efficiently precipitates over 99% neodymium (Nd), 99% dysprosium (Dy), and 98% lanthanum (La) from individual REE chloride solutions. Recovery from a low-grade ore leachate achieves over 99% total recovery. X-ray diffraction (XRD) and Fourier transform infrared spectroscopy (FTIR) confirm that REE oxalates precipitated with bio-oxalic acid closely resemble those obtained using commercial oxalic acid. Techno-economic analysis (TEA) and life cycle assessment (LCA) further demonstrate that bio-oxalic acid can be produced at a competitive price of $1.79·kg -1 while reducing carbon intensity (CI) by 112% to 63.5% with and without electricity displacement, respectively, relative to the fossil-based benchmark. These results highlight bio-oxalic acid as a green, economically viable alternative to synthetic oxalate for sustainable REE recovery.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Desiccation induces varied responses within a soil bacterial genus

Abstract Desiccation impacts a suite of physiological processes in microbes by elevating levels of damaging reactive oxygen species and inducing DNA strand breaks. In response to desiccation‐induced stress, microbes have evolved specialized mechanisms to help them survive. Here, we performed a 128‐day lab desiccation experiment on nine strains from three clades of an abundant soil bacterium, Curtobacterium . We sequenced RNA from each strain at three time points to investigate their response. Curtobacterium was highly resistant to desiccation, outlasting both Escherichia coli and a famously DNA damage‐resistant bacterium, Deinococcus radiodurans . However, within the genus, there were also 10‐fold differences in survival rates among strains. Transcriptomic profiling revealed responses shared within the genus including up‐regulation of genes involved in DNA damage repair, osmolyte production, and efflux pumps, but also up‐regulation of pathways and genes unique to the three clades. For example, trehalose synthesis gene otsB , the chaperone groEL , and the oxygen scavenger katA were all found in either one or two clades but not the third. Here, we provide evidence of considerable variation in closely related strains, and further elucidation of the phylogenetic conservation of desiccation tolerance remains an important goal for microbial ecologists.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Systems Analysis of the Physiological and Molecular Mechanisms of Sorghum Nitrogen Use Efficiency, Water Use Efficiency and Interactions with the Soil Microbiome (Final Report for DE-SC0014395)

The specific project objectives were to: 1) Conduct deep census surveys of root microbiomes concurrent with phenotypic characterizations of a diverse panel of sorghum genotypes across multiple years to define the microbes associated with the most productive lines under drought and low nitrogen conditions. 2) Associate systems-level genotypic, microbial, and environmental factors with improved sorghum performance using robust statistical approaches. 3) Develop culture collections of sorghum root/leaf associated microbes that recapitulate root-enriched sequences defined in the census. 4) Perform controlled environment experiments for in-depth characterization and hypothesis testing of G sorghum x G microbe x E interactions . Validate physiological mechanisms, map genetic loci for stress tolerance, and determine the persistence of optimal microbial strains under greenhouse and field conditions.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Identification and expression of small multidrug resistance transporters in early‐branching anaerobic fungi

Abstract Membrane‐embedded transporters impart essential functions to cells as they mediate sensing and the uptake and extrusion of nutrients, waste products, and effector molecules. Promiscuous multidrug exporters are implicated in resistance to drugs and antibiotics and are highly relevant for microbial engineers who seek to enhance the tolerance of cell factory strains to hydrophobic bioproducts. Here, we report on the identification of small multidrug resistance (SMR) transporters in early‐branching anaerobic fungi (Neocallimastigomycetes). The SMR class of transporters is commonly found in bacteria but has not previously been reported in eukaryotes. In this study, we show that SMR transporters from anaerobic fungi can be produced heterologously in the model yeast Saccharomyces cerevisiae , demonstrating the potential of these proteins as targets for further characterization. The discovery of these novel anaerobic fungal SMR transporters offers a promising path forward to enhance bioproduction from engineered microbial strains.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Intraspecific variability in root traits and edaphic conditions influence soil microbiomes across 12 switchgrass cultivars

Microbial communities help plants access nutrients and tolerate stress. Some microbiomes are specific to plant genotypes and, therefore, may contribute to intraspecific differences in plant growth and be a promising target for plant breeding. Switchgrass (Panicum virgatum L.) is a potential bioenergy crop with broad variation in yields and environmental responses; recent studies suggest that associations with distinct microbiomes may contribute to variation in cultivar yields. We used a common garden experiment to investigate variation in 12 mature switchgrass cultivar soil microbiomes and, further, to examine how root traits and soil conditions influence microbiome structure. Here, we found that average root diameter varied up to 33% among cultivars and that they associated with distinct soil microbiomes. Cultivar had a larger effect on the soil bacterial than fungal community, but both were strongly influenced by soil properties. Root traits had a weaker effect on microbiome structure, but root length contributed to variation in the fungal community. Unlike the soil communities, the root bacterial communities did not group by cultivar, based on a subset of samples. Microbial biomass carbon and nitrogen and the abundance of several dominant bacterial phyla varied between ecotypes, but overall the differences in soil microbiomes were greater among cultivars than between ecotypes. Our findings show that there is not one soil microbiome that applies to all switchgrass cultivars, or even to each ecotype. These subtle but significant differences in root traits, microbial biomass, and the abundance of certain soil bacteria could explain differences in cultivar yields and environmental responses.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Stress-tolerant non-conventional microbes enable next-generation chemical biosynthesis

Microbial chemical production is a rapidly growing industry, with much of the growth fueled by advances in synthetic biology. New approaches have enabled rapid strain engineering for the production of various compounds; however, translation to industry is often problematic because native phenotypes of model hosts prevent the design of new low-cost bioprocesses. Here, in this work, we argue for a new approach that leverages the native stress-tolerant phenotypes of non-conventional microbes that directly address design challenges from the outset. Growth at high temperature, high salt and solvent concentrations, and low pH can enable cost savings by reducing the energy required for product separation, bioreactor cooling, and maintaining sterile conditions. These phenotypes have the added benefit of allowing for the use of low-cost sugar and water resources. Non-conventional hosts are needed because these phenotypes are polygenic and thus far have proven difficult to recapitulate in the common hosts Escherichia coli and Saccharomyces cerevisiae.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗

DOE OSTI2023

Uncovering the dominant role of root metabolism in shaping rhizosphere metabolome under drought in tropical rainforest plants

Plant-soil-microbe interactions are crucial for driving rhizosphere processes that contribute to metabolite turnover and nutrient cycling. With the increasing frequency and severity of water scarcity due to climate warming, understanding how plant-mediated processes, such as root exudation, influence soil organic matter turnover in the rhizosphere is essential. In this study, we used 16S rRNA gene amplicon sequencing, rhizosphere metabolomics, and position-specific 13 C-pyruvate labeling to examine the effects of three different plant species (Piper auritum, Hibiscus rosa sinensis, and Clitoria fairchildiana) and their associated microbial communities on soil organic carbon turnover in the rhizosphere. Here, our findings indicate that in these tropical plants, the rhizosphere metabolome is primarily shaped by the response of roots to drought rather than direct shifts in the rhizosphere bacterial community composition. Specifically, the reduced exudation of plant roots had a notable effect on the metabolome of the rhizosphere of P. auritum, with less reliance on neighboring microbes. Contrary to P. auritum, H. rosa sinensis and C. fairchildiana experienced changes in their exudate composition during drought, causing alterations to the bacterial communities in the rhizosphere. This, in turn, had a collective impact on the rhizosphere's metabolome. Furthermore, the exclusion of phylogenetically distant microbes from the rhizosphere led to shifts in its metabolome. Additionally, C. fairchildiana appeared to be associated with only a subset of symbiotic bacteria under drought conditions. These results indicate that plant species-specific microbial interactions systematically change with the root metabolome. As roots respond to drought, their associated microbial communities adapt, potentially reinforcing the drought tolerance strategies of plant roots. These findings have significant implications for maintaining plant health and preference during drought stress and improving plant performance under climate change.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2026

Data for High Yield Production of 3-Hydroxypropionic Acid Using Issatchenkia orientalis

Biomanufacturing provides a more sustainable alternative to fossil-based chemical manufacturing. 3-Hydroxypropionic acid (3HP) is a top Department of Energy value-added chemical and precursor to bioplastics, yet cost-effective microbial production remains elusive. Here, we establish the acid-tolerant yeast Issatchenkia orientalis as a robust host for low-pH 3HP biosynthesis. Genome-scale modeling identifies the β-alanine pathway as optimal, offering the highest theoretical yield and lowest oxygen requirement. Thermodynamic analysis confirms its favorability under acidic conditions. Using sequence similarity network analysis, we discover highly active aspartate 1-decarboxylase (PAND), β-alanine-pyruvate aminotransferase (BAPAT), and 3HP dehydrogenase (YDFG), which significantly improve the pathway efficiency. Next, to further elevate the production, pathway optimization through multi-copy PAND integration, byproduct elimination (knockouts of pyruvate decarboxylase and glycerol-3-phosphate dehydrogenase), and reinforcement of aspartate flux by overexpression of pyruvate carboxylase and aspartate amino transferase improves the titer to 29 g/L in shake flasks. Fed-batch fermentation at pH 4 with low-cost corn steep liquor medium further increases the production to 92 g/L with 0.7 g/g yield and 0.55 g/L/h productivity. Techno-economic analysis indicates that such performance could potentially enable a financially viable process for sustainable acrylic acid production. This work establishes I. orientalis as a next-generation platform for cost-effective 3HP production and paves the way toward industrial commercialization.

Bioproducts↗

DOE OSTI2022

Trait relationships of fungal decomposers in response to drought using a dual field and laboratory approach

Abstract Decomposer fungi play a fundamental role in terrestrial ecosystem dynamics. In the southwestern United States, climate change is causing more frequent and severe droughts, which may alter fungal community composition and activity. Investigating relationships between fungal traits may improve the prediction of fungal responses to drought. In this dual field and laboratory experiment, we examine whether trade‐offs occur between traits associated with drought. Specifically, we test the hypothesis that fungi sort into lifestyles specializing in growth y ield, resource a cquisition, and drought s tress tolerance (“YAS” framework). For the field experiment, we constructed microbial “cages” containing sterilized litter and 1 of 10 fungal isolates. These cages were placed in long‐term drought and control plots in a southern Californian grassland for 6 and 12 months. We measured fungal hyphal length per unit litter mass loss for growth yield, the potential activities of four extracellular enzymes for resource acquisition, and the ability to grow in the drought versus control plots for drought stress tolerance. We compared these results with a laboratory microcosm experiment constructed with the same fungal isolates and that measured the same fungal traits. The field experiment corroborated our laboratory results, in that no trade‐offs were observed between growth yield and resource acquisition traits. However, in contrast to the laboratory experiment, drought tolerance was negatively related to extracellular enzyme activity and growth yield in the field, implying a trade‐off. Despite this observed trade‐off in the field, growth yield was not hindered by drought. We propose a modification to the YAS framework, by combining the growth yield and resource acquisition lifestyles, which may be more appropriate for this arid system. This joint laboratory and field approach contextualizes a theoretical framework in microbial ecology and improves understanding of fungal community response to climate change.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Pre-Bleaching Coral Microbiome Is Enriched in Beneficial Taxa and Functions

Coral reef health is tightly connected to the coral holobiont, which is the association between the coral animal and a diverse microbiome functioning as a unit. The coral holobiont depends on key services such as nitrogen and sulfur cycling mediated by the associated bacteria. However, these microbial services may be impaired in response to environmental changes, such as thermal stress. A perturbed microbiome may lead to coral bleaching and disease outbreaks, which have caused an unprecedented loss in coral cover worldwide, particularly correlated to a warming ocean. The response mechanisms of the coral holobiont under high temperatures are not completely understood, but the associated microbial community is a potential source of acquired heat-tolerance. Here we investigate the effects of increased temperature on the taxonomic and functional profiles of coral surface mucous layer (SML) microbiomes in relationship to coral–algal physiology. We used shotgun metagenomics in an experimental setting to understand the dynamics of microbial taxa and genes in the SML microbiome of the coral Pseudodiploria strigosa under heat treatment. The metagenomes of corals exposed to heat showed high similarity at the level of bacterial genera and functional genes related to nitrogen and sulfur metabolism and stress response. The coral SML microbiome responded to heat with an increase in the relative abundance of taxa with probiotic potential, and functional genes for nitrogen and sulfur acquisition. Coral–algal physiology significantly explained the variation in the microbiome at taxonomic and functional levels. These consistent and specific microbial taxa and gene functions that significantly increased in proportional abundance in corals exposed to heat are potentially beneficial to coral health and thermal resistance.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Chronic drought differentially alters the belowground microbiome of drought tolerant and drought susceptible genotypes of Populus trichocarpa

Populus trichocarpa is an ecologically important tree species and economically important biofeedstock. Belowground, P. trichocarpa interacts with diverse microorganisms in the rhizosphere and root endosphere. These plant-microbial interactions can bolster a variety of plant processes, ranging from pathogen suppression to drought tolerance, yet we know little about the impact of chronic drought stress on P. trichocarpa’s belowground microbiomes. To investigate the interactive effect of chronic drought on belowground microbial communities across genetically different P. trichocarpa hosts, we assessed archaeal/bacterial and fungal communities within the root endosphere, rhizosphere, and surrounding bulk soil of selected genotypes in a long-term drought experiment in Boardman, OR, USA. We sequenced the 16S rRNA and ITS2 gene region on samples collected from 16 distinct P. trichocarpa genotypes in plots with full or reduced irrigation. Eight of these genotypes have been previously identified as drought tolerant while the other eight genotypes were drought susceptible. While reduced irrigation influenced the composition of every archaeal/bacterial microbiome compartment, fungal communities were only affected in the rhizosphere and bulk soil compartments. Drought-tolerant bacteria, such as Actinobacteria, were differentially abundant in reduced irrigation across all belowground microbiomes. Host drought-tolerance influenced plant-associated microbiome compartments but had little impact on the bulk soil compartment. Drought-tolerant trees were enriched for potential growth-promoting microorganisms in the root endosphere and rhizosphere, including Sphingomonas bacteria and ectomycorrhizal fungi. Overall, associations of growth-promoting microbes in drought resistant P. trichocarpa genotypes can be leveraged to improve biofeedstock productivity in regions prone to periodic drought.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

RB-TnSeq identifies genetic targets for improved tolerance of Pseudomonas putida towards compounds relevant to lignin conversion

We report lignin-derived mixtures intended for bioconversion commonly contain high concentrations of aromatic acids, aliphatic acids, and salts. The inherent toxicity of these chemicals places a significant bottleneck upon the effective use of microbial systems for the valorization of these mixtures. Pseudomonas putida KT2440 can tolerate stressful quantities of several lignin-related compounds, making this bacterium a promising host for converting these chemicals to valuable bioproducts. Nonetheless, further increasing P. putida tolerance to chemicals in lignin-rich substrates has the potential to improve bioprocess performance. Accordingly, we employed random barcoded transposon insertion sequencing (RB-TnSeq) to reveal genetic determinants in P. putida KT2440 that influence stress outcomes during exposure to representative constituents found in lignin-rich process streams. The fitness information obtained from the RB-TnSeq experiments informed engineering of strains via deletion or constitutive expression of several genes. Namely, ΔgacAS, ΔfleQ, ΔlapAB, ΔttgR::P tac :ttgABC, Ptac:PP_1150:PP_1152, ..delta..relA, and ΔPP_1430 mutants showed growth improvement in the presence of single compounds, and some also exhibited greater tolerance when grown using a complex chemical mixture representative of a lignin-rich chemical stream. Overall, this work demonstrates the successful implementation of a genome-scale screening tool for the identification of genes influencing stress tolerance against notable compounds within lignin-enriched chemical streams, and the genetic targets identified herein offer promising engineering targets for improving feedstock tolerance in lignin valorization strains of P. putida KT2440.

09 BIOMASS FUELS↗

DOE OSTI2023

Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils

Abstract Peatlands are among the largest natural sources of atmospheric methane (CH 4 ) worldwide. Microbial processes play a key role in regulating CH 4 emissions from peatland ecosystems, yet the complex interplay between soil substrates and microbial communities in controlling CH 4 emissions as a function of global change remains unclear. Herein, we performed an integrated analysis of multi‐omics data sets to provide a comprehensive understanding of the molecular processes driving changes in greenhouse gas (GHG) emissions in peatland ecosystems with increasing temperature and sulfate deposition in a laboratory incubation study. We sought to first investigate how increasing temperatures (4, 21, and 35°C) impact soil microbiome–metabolome interactions; then explore the competition between methanogens and sulfate‐reducing bacteria (SRBs) with increasing sulfate concentrations at the optimum temperature for methanogenesis. Our results revealed that peat soil organic matter degradation, mediated by biotic and potentially abiotic processes, is the main driver of the increase in CO 2 production with temperature. In contrast, the decrease in CH 4 production at 35°C was linked to the absence of syntrophic communities and the potential inhibitory effect of phenols on methanogens. Elevated temperatures further induced the microbial communities to develop high growth yield and stress tolerator trait‐based strategies leading to a shift in their composition and function. On the other hand, SRBs were able to outcompete methanogens in the presence of non‐limiting sulfate concentrations at 21°C, thereby reducing CH 4 emissions. At higher sulfate concentrations, however, the prevalence of communities capable of producing sufficient low‐molecular‐weight carbon substrates for the coexistence of SRBs and methanogens was translated into elevated CH 4 emissions. The use of omics in this study enhanced our understanding of the structure and interactions among microbes with the abiotic components of the system that can be useful for mitigating GHG emissions from peatland ecosystems in the face of global change.

AminiTabrizi, Roya↗

DOE OSTI2024

Increasing Bacterial Tolerance and Metabolism of the Biofuel, N-Butanol Using Community-Level Evolution and Functional Genomics

Bioremediation capability should be developed along with biofuel technology to mitigate the potential damage of future spills. One biofuel that is being developed is biobutanol, since n-butanol is more energy dense and less volatile than ethanol. A bottleneck for industrial production of biobutanol is its toxicity; most microbes cannot survive about 1.5% v/v. Thus, microbial bioremediation of n-butanol would need microbes that can both tolerate and metabolize butanol. We used ecological and evolutionary biology approaches to find bacteria that could tolerate and metabolize butanol. We then tried to increase the metabolism of butanol by promising bacterial strains and communities. Ecological community-level assays and screenings were conducted followed by 16S amplicon sequencing to identify butanol-tolerant artificial bacterial communities. Promising communities were then tested for growth with butanol as the sole carbon source. Secondly, we looked for bacteria with alcohol dehydrogenase enzymes and looked to increase butanol metabolism. We found that the tolerance for n-butanol may be improved with repeated exposure, but it was difficult to switch from tolerance to metabolism. Bacterial community v dynamics may be influenced by n-butanol concentration, and there was putative butanol metabolism found with both research approaches.

09 BIOMASS FUELS↗

DOE OSTI2026

High yield production of 3-hydroxypropionic acid using Issatchenkia orientalis

Biotechnology↗