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DOE OSTI2021

Structural Basis of Ligand Selectivity by a Bacterial Adhesin Lectin Involved in Multispecies Biofilm Formation

Carbohydrate recognition by lectins governs critical host-microbe interactions. MpPA14 (Marinomonas primoryensis PA14 domain) lectin is a domain of a 1.5-MDa adhesin responsible for a symbiotic bacterium-diatom interaction in Antarctica. Here, we show that MpPA14 binds various monosaccharides, with l-fucose and N-acetylglucosamine being the strongest ligands (dissociation constant [K d ], ~150 μM). High-resolution structures of MpPA14 with 15 different sugars bound elucidated the molecular basis for the lectin’s apparent binding promiscuity but underlying selectivity. MpPA14 mediates strong Ca 2+ -dependent interactions with the 3,4-diols of l-fucopyranose and glucopyranoses, and it binds other sugars via their specific minor isomers. Thus, MpPA14 only binds polysaccharides like branched glucans and fucoidans with these free end groups. Consistent with our findings, adhesion of MpPA14 to diatom cells was selectively blocked by l-fucose, but not by N-acetyl galactosamine. The MpPA14 lectin homolog present in a Vibrio cholerae adhesin was produced and was shown to have the same sugar binding preferences as MpPA14. The pathogen’s lectin was unable to effectively bind the diatom in the presence of fucose, thus demonstrating the antiadhesion strategy of blocking infection via ligand-based antagonists.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome

Symbiotic mutualisms of bacteria and animals are ubiquitous in nature, running a continuum from facultative to obligate from the perspectives of both partners. The loss of functions required for living independently but not within a host gives rise to reduced genomes in many symbionts. Although the phenomenon of genome reduction can be explained by existing evolutionary models, the initiation of the process is not well understood. Here, we describe the microbiome associated with the eggs of the beetle Lagria villosa, consisting of multiple bacterial symbionts related to Burkholderia gladioli, including a reduced-genome symbiont thought to be the exclusive producer of the defensive compound lagriamide. We show that the putative lagriamide-producing symbiont is the only member of the microbiome undergoing genome reduction and that it has already lost the majority of its primary metabolism and DNA repair pathways. The key step preceding genome reduction in the symbiont was likely the horizontal acquisition of the putative lagriamide lga biosynthetic gene cluster. Unexpectedly, we uncovered evidence of additional horizontal transfers to the symbiont’s genome while genome reduction was occurring and despite a current lack of genes needed for homologous recombination. These gene gains may have given the genome-reduced symbiont a selective advantage in the microbiome, especially given the maintenance of the large lga gene cluster despite ongoing genome reduction.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

The Roseibium album (Labrenzia alba) Genome Possesses Multiple Symbiosis Factors Possibly Underpinning Host-Microbe Relationships in the Marine Benthos

Here, we announce the genomes of eight Roseibium album (synonym Labrenzia alba ) strains that were obtained from the octocoral Eunicella labiata . Genome annotation revealed multiple symbiosis factors common to all genomes, such as eukaryotic-like repeat protein- and multidrug resistance-encoding genes, which likely underpin symbiotic relationships with marine invertebrate hosts.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Construction and Modeling of a Coculture Microplate for Real-Time Measurement of Microbial Interactions

The dynamic structures of microbial communities emerge from the complex network of interactions between their constituent microorganisms. Quantitative measurements of these interactions are important for understanding and engineering ecosystem structure. Here, we present the development and application of the BioMe plate, a redesigned microplate device in which pairs of wells are separated by porous membranes. BioMe facilitates the measurement of dynamic microbial interactions and integrates easily with standard laboratory equipment. We first applied BioMe to recapitulate recently characterized, natural symbiotic interactions between bacteria isolated from the Drosophila melanogaster gut microbiome. Specifically, the BioMe plate allowed us to observe the benefit provided by two Lactobacillus strains to an Acetobacter strain. We next explored the use of BioMe to gain quantitative insight into the engineered obligate syntrophic interaction between a pair of Escherichia coli amino acid auxotrophs. We integrated experimental observations with a mechanistic computational model to quantify key parameters associated with this syntrophic interaction, including metabolite secretion and diffusion rates. This model also allowed us to explain the slow growth observed for auxotrophs growing in adjacent wells by demonstrating that, under the relevant range of parameters, local exchange between auxotrophs is essential for efficient growth. The BioMe plate provides a scalable and flexible approach for the study of dynamic microbial interactions.

3D printed device↗

DOE OSTI2023

Inorganic sulfate-based signatures of chemosymbiosis in modern infaunal lucinids

Bivalves that host sulfur-oxidizing bacterial gill-hosted endosymbionts can inhabit low-diversity, sulfidic environmental niches. However, understanding the history of this life strategy is limited by the lack of a robust method that can be applied to fossils. Measurements of carbonate-associated sulfate S isotope ratios (CAS-$δ$ 34 S) in carbonate fossils could fill this void by fingerprinting symbiont-driven oxidation of environmental sulfide. We begin to evaluate this prediction using modern lucinid bivalves, a useful test case because: (1) all modern genera host symbionts and live in sulfidic sediments, and (2) morphological evidence suggests that this has been true since the earliest ancestral lucinids. We measured S speciation, abundance, and CAS-$δ$ 34 S values in the shells of a suite of modern infaunal lucinids, in addition to epifaunal bivalves with and without S-oxidizing symbionts as controls. For infaunal lucinids, CAS concentrations were at most one-third of those of non-symbiotic epifaunal bivalves, and CAS-$δ$ 34 S values were lower (9.2‰-18.5‰) than in modern seawater (21‰) or epifaunal bivalves (20.8‰-21‰). These observations indicate that lucinids with symbionts incorporate sulfide-derived sulfate into their shells as a direct consequence of their chemosymbiosis. In conclusion, we argue that both the concentration and the magnitude of 34 S depletion in infaunal lucinid CAS reflect environmental sulfide concentrations and could viably reveal chemosymbiosis in fossils.

58 GEOSCIENCES↗

DOE OSTI2021

A Century of Synergy in Termite Symbiosis Research: Linking the Past with New Genomic Insights

Termites have long been studied for their symbiotic associations with gut microbes. In the late nineteenth century, this relationship was poorly understood and captured the interest of parasitologists such as Joseph Leidy; this research led to that of twentieth-century biologists and entomologists including Cleveland, Hungate, Trager, and Lüscher. Early insights came via microscopy, organismal, and defaunation studies, which led to descriptions of microbes present, descriptions of the roles of symbionts in lignocellulose digestion, and early insights into energy gas utilization by the host termite. Focus then progressed to culture-dependent microbiology and biochemical studies of host–symbiont complementarity, which revealed specific microhabitat requirements for symbionts and noncellulosic mechanisms of symbiosis (e.g., N 2 fixation). Today, knowledge on termite symbiosis has accrued exponentially thanks to omic technologies that reveal symbiont identities, functions, and interdependence, as well as intricacies of host–symbiont complementarity. Moving forward, the merging of classical twentieth-century approaches with evolving omic tools should provide even deeper insights into host–symbiont interplay.

Entomology↗

DOE OSTI2021

Berkeley Quantum Synthesis Toolkit (BQSKit) v1

The Berkeley Quantum Synthesis Toolkit (BQSKit) is an optimizing quantum compiler and research vehicle that combines ideas from several projects at LBNL into one easily accessible and quickly extensible software package. The ideas in the QFAST, QSearch, LEAP, and QFactor software tools (all licensed through ipo.lbl.gov) all build upon one another. By combining these into one package, we create symbiotic interactions between the tools. This means better results, better throughput, less to maintain, and greater surface area to the public. Additionally, the BQSKit tool will create a research platform for future work here at LBNL.

Younis, Ed↗

DOE OSTI2022

Identification of microRNAs responsive to arbuscular mycorrhizal fungi in Panicum virgatum (switchgrass)

Background: MicroRNAs (miRNAs) are important post-transcriptional regulators involved in the control of a range of processes, including symbiotic interactions in plants. MiRNA involvement in arbuscular mycorrhizae (AM) symbiosis has been mainly studied in model species, and our study is the first to analyze global miRNA expression in the roots of AM colonized switchgrass ( Panicum virgatum ), an emerging biofuel feedstock. AM symbiosis helps plants gain mineral nutrition from the soil and may enhance switchgrass biomass production on marginal lands. Our goals were to identify miRNAs and their corresponding target genes that are controlling AM symbiosis in switchgrass. Results: Through genome-wide analysis of next-generation miRNA sequencing reads generated from switchgrass roots, we identified 122 mature miRNAs, including 28 novel miRNAs. By comparing miRNA expression profiles of AM-inoculated and control switchgrass roots, we identified 15 AM-responsive miRNAs across lowland accession “Alamo”, upland accession “Dacotah”, and two upland/lowland F 1 hybrids. We used degradome sequencing to identify target genes of the AM-responsive miRNAs revealing targets of miRNAs residing on both K and N subgenomes. Notably, genes involved in copper ion binding were targeted by downregulated miRNAs, while upregulated miRNAs mainly targeted GRAS family transcription factors. Conclusion: Through miRNA analysis and degradome sequencing, we revealed that both upland and lowland switchgrass genotypes as well as upland-lowland hybrids respond to AM by altering miRNA expression. We demonstrated complex GRAS transcription factor regulation by the miR171 family, with some miR171 family members being AM responsive while others remained static. Copper miRNA downregulation was common amongst the genotypes tested and we identified superoxide dismutases and laccases as targets, suggesting that these Cu-miRNAs are likely involved in ROS detoxification and lignin deposition, respectively. Other prominent targets of the Cu miRNAs were blue copper proteins. Overall, the potential effect of AM colonization on lignin deposition pathways in this biofuel crop highlights the importance of considering AM and miRNA in future biofuel crop development strategies.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Genetic variation and genetic complexity of nodule occupancy in soybean inoculated with USDA110 and USDA123 rhizobium strains

Abstract Background Symbiotic nitrogen fixation differs among Bradyrhizobium japonicum strains. Soybean inoculated with USDA123 has a lower yield than strains known to have high nitrogen fixation efficiency, such as USDA110. In the main soybean-producing area in the Midwest of the United States, USDA123 has a high nodule incidence in field-grown soybean and is competitive but inefficient in nitrogen fixation. In this study, a high-throughput system was developed to characterize nodule number among 1,321 Glycine max and 69 Glycine soja accessions single inoculated with USDA110 and USDA123. Results Seventy-three G. max accessions with significantly different nodule number of USDA110 and USDA123 were identified. After double inoculating 35 of the 73 accessions, it was observed that PI189939, PI317335, PI324187B, PI548461, PI562373, and PI628961 were occupied by USDA110 and double-strain nodules but not by USDA123 nodules alone. PI567624 was only occupied by USDA110 nodules, and PI507429 restricted all strains. Analysis showed that 35 loci were associated with nodule number in G. max when inoculated with strain USDA110 and 35 loci with USDA123. Twenty-three loci were identified in G. soja when inoculated with strain USDA110 and 34 with USDA123. Only four loci were common across two treatments, and each locus could only explain 0.8 to 1.5% of phenotypic variation. Conclusions High-throughput phenotyping systems to characterize nodule number and occupancy were developed, and soybean germplasm restricting rhizobium strain USDA123 but preferring USDA110 was identified. The larger number of minor effects and a small few common loci controlling the nodule number indicated trait genetic complexity and strain-dependent nodulation restriction. The information from the present study will add to the development of cultivars that limit USDA123, thereby increasing nitrogen fixation efficiency and productivity.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Metabolic dependencies govern microbial syntrophies during methanogenesis in an anaerobic digestion ecosystem

Methanogenesis, a biological process mediated by complex microbial communities, has attracted great attention due to its contribution to global warming and potential in biotechnological applications. The current study unveiled the core microbial methanogenic metabolisms in anaerobic vessel ecosystems by applying combined genome-centric metagenomics and metatranscriptomics. Here, we demonstrate that an enriched natural system, fueled only with acetate, could support a bacteria-dominated microbiota employing a multi-trophic methanogenic process. Moreover, significant changes, in terms of microbial structure and function, were recorded after the system was supplemented with additional H 2 . Methanosarcina thermophila, the predominant methanogen prior to H 2 addition, simultaneously performed acetoclastic, hydrogenotrophic, and methylotrophic methanogenesis. The methanogenic pattern changed after the addition of H 2 , which immediately stimulated Methanomicrobia-activity and was followed by a slow enrichment of Methanobacteria members. Interestingly, the essential genes involved in the Wood-Ljungdahl pathway were not expressed in bacterial members. The high expression of a glycine cleavage system indicated the activation of alternative metabolic pathways for acetate metabolism, which were reconstructed in the most abundant bacterial genomes. Moreover, as evidenced by predicted auxotrophies, we propose that specific microbes of the community were forming symbiotic relationships, thus reducing the biosynthetic burden of individual members. These results provide new information that will facilitate future microbial ecology studies of interspecies competition and symbiosis in methanogenic niches.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Metagenomic insights into the taxonomy, function, and dysbiosis of prokaryotic communities in octocorals

Background. In octocorals (Cnidaria Octocorallia), the functional relationship between host health and its symbiotic consortium has yet to be determined. Here, we employed comparative metagenomics to uncover the distinct functional and phylogenetic features of the microbiomes of healthy Eunicella gazella, Eunicella verrucosa, and Leptogorgia sarmentosa tissues, in contrast with the microbiomes found in seawater and sediments. We further explored how the octocoral microbiome shifts to a pathobiome state in E. gazella. Results. Multivariate analyses based on 16S rRNA genes, Clusters of Orthologous Groups of proteins (COGs), Protein families (Pfams), and secondary metabolite-biosynthetic gene clusters annotated from 20 Illumina-sequenced metagenomes each revealed separate clustering of the prokaryotic communities of healthy tissue samples of the three octocoral species from those of necrotic E. gazella tissue and surrounding environments. While the healthy octocoral microbiome was distinguished by so-far uncultivated Endozoicomonadaceae, Oceanospirillales, and Alteromonadales phylotypes in all host species, a pronounced increase of Flavobacteriaceae and Alphaproteobacteria, originating from seawater, was observed in necrotic E. gazella tissue. Increased abundances of eukaryotic-like proteins, exonucleases, restriction endonucleases, CRISPR/Cas proteins, and genes encoding for heat-shock proteins, inorganic ion transport, and iron storage distinguished the prokaryotic communities of healthy octocoral tissue regardless of the host species. An increase of arginase and nitric oxide reductase genes, observed in necrotic E. gazella tissues, suggests the existence of a mechanism for suppression of nitrite oxide production by which octocoral pathogens may overcome the host’s immune system. Conclusions. This is the first study to employ primer-less, shotgun metagenome sequencing to unveil the taxonomic, functional, and secondary metabolism features of prokaryotic communities in octocorals. Our analyses reveal that the octocoral microbiome is distinct from those of the environmental surroundings, is host genus (but not species) specific, and undergoes large, complex structural changes in the transition to the dysbiotic state. Host-symbiont recognition, abiotic-stress response, micronutrient acquisition, and an antiviral defense arsenal comprising multiple restriction endonucleases, CRISPR/Cas systems, and phage lysogenization regulators are signatures of prokaryotic communities in octocorals. We argue that these features collectively contribute to the stabilization of symbiosis in the octocoral holobiont and constitute beneficial traits that can guide future studies on coral reef conservation and microbiome therapy.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi

Abstract Background Linking the identity of wild microbes with their ecophysiological traits and environmental functions is a key ambition for microbial ecologists. Of many techniques that strive for this goal, Stable-isotope probing—SIP—remains among the most comprehensive for studying whole microbial communities in situ. In DNA-SIP, actively growing microorganisms that take up an isotopically heavy substrate build heavier DNA, which can be partitioned by density into multiple fractions and sequenced. However, SIP is relatively low throughput and requires significant hands-on labor. We designed and tested a semi-automated, high-throughput SIP (HT-SIP) pipeline to support well-replicated, temporally resolved amplicon and metagenomics experiments. We applied this pipeline to a soil microhabitat with significant ecological importance—the hyphosphere zone surrounding arbuscular mycorrhizal fungal (AMF) hyphae. AMF form symbiotic relationships with most plant species and play key roles in terrestrial nutrient and carbon cycling. Results Our HT-SIP pipeline for fractionation, cleanup, and nucleic acid quantification of density gradients requires one-sixth of the hands-on labor compared to manual SIP and allows 16 samples to be processed simultaneously. Automated density fractionation increased the reproducibility of SIP gradients compared to manual fractionation, and we show adding a non-ionic detergent to the gradient buffer improved SIP DNA recovery. We applied HT-SIP to 13 C-AMF hyphosphere DNA from a 13 CO 2 plant labeling study and created metagenome-assembled genomes (MAGs) using high-resolution SIP metagenomics (14 metagenomes per gradient). SIP confirmed the AMF Rhizophagus intraradices and associated MAGs were highly enriched (10–33 atom% 13 C), even though the soils’ overall enrichment was low (1.8 atom% 13 C). We assembled 212 13 C-hyphosphere MAGs; the hyphosphere taxa that assimilated the most AMF-derived 13 C were from the phyla Myxococcota, Fibrobacterota, Verrucomicrobiota, and the ammonia-oxidizing archaeon genus Nitrososphaera . Conclusions Our semi-automated HT-SIP approach decreases operator time and improves reproducibility by targeting the most labor-intensive steps of SIP—fraction collection and cleanup. We illustrate this approach in a unique and understudied soil microhabitat—generating MAGs of actively growing microbes living in the AMF hyphosphere (without plant roots). The MAGs’ phylogenetic composition and gene content suggest predation, decomposition, and ammonia oxidation may be key processes in hyphosphere nutrient cycling.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

The gut microbiome mediates adaptation to scarce food in Coleoptera

Beetles are ubiquitous cave invertebrates worldwide that adapted to scarce subterranean resources when they colonized caves. Here, we investigated the potential role of gut microbiota in the adaptation of beetles to caves from different climatic regions of the Carpathians. The beetles’ microbiota was host-specific, reflecting phylogenetic and nutritional adaptation. The microbial community structure further resolved conspecific beetles by caves suggesting microbiota-host coevolution and influences by local environmental factors. The detritivore species hosted a variety of bacteria known to decompose and ferment organic matter, suggesting turnover and host cooperative digestion of the sedimentary microbiota and allochthonous-derived nutrients. The cave Carabidae, with strong mandibula, adapted to predation and scavenging of animal and plant remains, had distinct microbiota dominated by symbiotic lineages Spiroplasma or Wolbachia. All beetles had relatively high levels of fermentative Carnobacterium and Vagococcus involved in lipid accumulation and a reduction of metabolic activity, and both features characterize adaptation to caves.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Plot and Tree Characteristics from the 2022-2023 field experiment at Game Ridge, Missoula County, Montana, USA

This dataset contains plot and study tree characteristics including identifiers, latitude and longitude data, tree heights, tree diameters, and distance between trees within a study plot. Data files and data dictionary(ies) are uploaded as .csv files and .xlsx files. The Users Guide is a .pdf file. Location data can be found in the Google Earth file GameRidge_SitePlotCoordinates.kmz.kml included here. These datasets were collected for Plant Carbohydrate Depletion, Mycorrhizal Networks, and Vulnerability to Drought: An Experimental Test in the Field. This experiment examined the interdependency between plant hydraulics and carbohydrate availability and sought to develop ways to incorporate interactions with below ground symbiotic organisms to better model and quantify forest response to drought. This environmental data was collected to provide context for the fungal community data and Pinus ponderosa physiological data.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Pinus ponderosa physiology data from the 2022 shade manipulation field experiment at Game Ridge, Missoula County, Montana, USA

This dataset contains physiology data on Pinus ponderosa saplings, including: leaf water potential (MPa, megapascals), leaf osmotic potential (MPa, megapascals), leaf pressure potential (MPa, megapascals), leaf relative water content (% saturated mass), as well as soluble sugars (% dry mass),starch (% dry mass), and total nonstructural carbohydrates (% dry mass) found in branch phloem and xylem. Data files and data dictionary(ies) are uploaded as .csv files and .xlsx files. The Users Guide is a .pdf file. Location data can be found in the Google Earth file GameRidge_SitePlotCoordinates.kmz.kml included here. These datasets were collected for Plant Carbohydrate Depletion, Mycorrhizal Networks, and Vulnerability to Drought: An Experimental Test in the Field. This experiment examined the interdependency between plant hydraulics and carbohydrate availability and sought to develop ways to incorporate interactions with below ground symbiotic organisms to better model and quantify forest response to drought.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Pinus ponderosa physiology data from the 2023 girdling manipulation field experiment at Game Ridge, Missoula County, Montana, USA

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2024

Environmental monitoring data from the 2022-2023 field experiment at Game Ridge, Missoula County, Montana, USA

This dataset contains sensor data from programmed loggers as well as handheld moisture probes, including weather data, air and soil temperature, and soil volumetric water content. Data files and data dictionary(ies) are uploaded as .csv files. The Users Guide is a .pdf file. Location data can be found in the Google Earth file GameRidge_SitePlotCoordinates.kmz.kml included here. These datasets were collected for Plant Carbohydrate Depletion, Mycorrhizal Networks, and Vulnerability to Drought: An Experimental Test in the Field. This experiment examined the interdependency between plant hydraulics and carbohydrate availability and sought to develop ways to incorporate interactions with below ground symbiotic organisms to better model and quantify forest response to drought. This environmental data was collected to provide context for the fungal community data and Pinus ponderosa physiological data.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2020

Description of the LASSO Data Bundles Product

The U. S. Department of Energy (DOE) Atmospheric Radiation Measurement (ARM) user facility began a pilot project in May 2015 to design a routine, high-resolution modeling capability to complement ARM’s extensive suite of measurements. This modeling capability has evolved into the Large-Eddy Simulation (LES) ARM Symbiotic Simulation and Observation (LASSO) datastream. The datastream, broadly termed data bundles, contains high-resolution model output, input files, observations for evaluation, and skill scores for the simulations. The initial focus of LASSO is on shallow convection at the ARM Southern Great Plains (SGP) atmospheric observatory. The availability of LES simulations with concurrent observations serves many purposes. LES helps bridge the scale gap between DOE ARM observations and models, and the use of routine LES adds value to observations. It provides a self-consistent representation of the atmosphere and a dynamical context for the observations. Further, it elucidates unobservable processes and properties. LASSO generates a simulation library for researchers that enables statistical approaches beyond a single-case mentality. It also provides tools necessary for modelers to reproduce the LES and conduct their own sensitivity experiments. The LASSO library of data bundles is designed to facilitate a wide range of research. For an observationalist, LASSO can help inform instrument remote-sensing retrievals, conduct observation system simulation experiments (OSSEs), and test implications of radar scan strategies or flight paths. For a theoretician, LASSO can help calculate estimates of fluxes and co-variability of values, and test relationships without having to run the model personally. For a modeler, LASSO can help one know ahead of time which days have good forcing, have co-registered observations at high-resolution scales, and have simulation inputs and corresponding outputs to test parameterizations. Further details on the overall LASSO project are available at https://www.arm.gov/capabilities/modeling/lasso.

54 ENVIRONMENTAL SCIENCES↗