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All sourcesNASA NTRSDOE OSTI
DOE OSTI2022

Pichia sp. yHMH446 translation elongation factor 1-alpha gene, partial cds

A novel budding yeast species was isolated from a soil sample collected in the United States of America. Phylogenetic analyses of multiple loci and phylogenomic analyses conclusively placed the species within the genus Pichia. Strain yHMH446 falls within a clade that includes Pichia norvegensis, Pichia pseudocactophila, Candida inconspicua, and Pichia cactophila. Whole genome sequence data were analyzed for the presence of genes known to be important for carbon and nitrogen metabolism, and the phenotypic data from the novel species were compared to all Pichia species with publicly available genomes. Across the genus, including the novel species candidate, we found that the inability to use many carbon and nitrogen sources correlated with the absence of metabolic genes. Based on these results, Pichia galeolata sp. nov. is proposed to accommodate yHMH446(T) (=NRRL Y-64187 = CBS 16864). This study shows how integrated taxogenomic analysis can add mechanistic insight to species descriptions.

genome sequence↗
DOE OSTI2022

GROWdb US River Systems - Samples

GROW Overview We developed the Genome Resolved Open Watersheds database (GROWdb), which aims to increase genomic sampling and understanding of global river microbiomes. An emphasis of GROWdb is to create a publicly available and ever-expanding microbial genome database that is focused on rivers while being interoperable with databases from other ecosystems. GROWdb is based on a network-of-networks approach to move beyond a small collection of well-studied rivers, towards a spatially distributed, global network of systematic observations. GROWdb represents the first microbial, river-focused resource parsed at various scales from genes to MAGs to community level including expression and potential based measurements that will be of interest to microbiologists, ecologists, geochemists, hydrologists, and modelers. Dataset Acknowledgement GROWdb contains data from various research campaigns, please acknowledge the following data generators, as appropriate: WHONDRS derived genomes or samples - include this statement in your acknowledgements: “This study used data from the Worldwide Hydrobiogeochemistry Observation Network for Dynamic River Systems (WHONDRS) under the River Corridor Science Focus Area (SFA) at the Pacific Northwest National Laboratory (PNNL) that was generated at the U.S. Department of Energy (DOE) Joint Genome Institute User Facility. PNNL is operated by Battelle Memorial Institute for the U.S. DOE under Contract No. DE-AC05-76RL01830. The SFA is supported by the U.S. DOE, Office of Biological and Environmental Research (BER), Environmental System Science (ESS) Program.” Total Samples loaded onto this Narrative: 178 Note: Not all GROW samples may be loaded into KBase Data Availability The data underlying GROWdb are accessible across various platforms to ensure all levels of data structure are widely available. First, all reads and MAGs are publicly hosted on National Center for Biotechnology (NCBI) under Bioproject PRJNA946291. Second, all data related data presented here including MAG annotations, extended data tables, phylogenetic tree files, antibiotic resistance gene database files, and MAG abundance tables are available in Zenodo (link). Beyond the flat database files listed above, our aim for GROWdb was to maximize data use by making the data available in searchable and interactive platforms including the National Microbiome Data Collaborative (NMDC) data portal, the Department of Energy’s Systems Biology Knowledgebase (KBase), and a GROW specific user interface released here, GROWdb Explorer. Each platform provides different ways to interact with GROWdb: NMDC GROWdb formed a pilot project for the NMDC. Specifically, individual GROWdb datasets (metagenomes, metatranscriptomes, etc) are easily accessible and searchable through the NMDC data portal, where they are systematically connected to each other and to a rich suite of sample information and standard analysis results, following Findable, Accessible, Interoperable, and Reusable (FAIR) data practices. KBase GROWdb is publicly available within KBase, including samples (this Narrative), MAGs, and corresponding genome scale metabolic models. Access within KBase allows for immediate access and reuse of data, including comparison to private data using KBase’s 500+ analysis tools. Other linked narratives in KBase: GROW Metagenome Assembled Genomes (MAGs) GROW Metabolic Models GROWdb Explorer GROWdb data is also explorable through a graphical user interface built through the Colorado State University Geospatial Centroid (https://geocentroid.shinyapps.io/GROWdatabase/), allowing users to search and graph microbial and spatial data simultaneously. In summary, this microbial genome resource represents the first publicly available genome collection from rivers and offers data that can be leveraged across microbiome studies. GROWdb is an expanding repository to incorporate and unify global river multi-omic data for the future.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

The histone code of the fungal genus Aspergillus uncovered by evolutionary and proteomic analyses

Chemical modifications of DNA and histone proteins impact the organization of chromatin within the nucleus. Changes in these modifications, catalysed by different chromatin-modifying enzymes, influence chromatin organization, which in turn is thought to impact the spatial and temporal regulation of gene expression. While combinations of different histone modifications, the histone code, have been studied in several model species, we know very little about histone modifications in the fungal genus Aspergillus, whose members are generally well studied due to their importance as models in cell and molecular biology as well as their medical and biotechnological relevance. Here, we used phylogenetic analyses in 94 Aspergilli as well as other fungi to uncover the occurrence and evolutionary trajectories of enzymes and protein complexes with roles in chromatin modifications or regulation. We found that these enzymes and complexes are highly conserved in Aspergilli, pointing towards a complex repertoire of chromatin modifications. Nevertheless, we also observed few recent gene duplications or losses, highlighting Aspergillus species to further study the roles of specific chromatin modifications. SET7 (KMT6) and other components of PRC2 (Polycomb Repressive Complex 2), which is responsible for methylation on histone H3 at lysine 27 in many eukaryotes including fungi, are absent in Aspergilli as well as in closely related Penicillium species, suggesting that these lost the capacity for this histone modification. We corroborated our computational predictions by performing untargeted MS analysis of histone post-translational modifications in Aspergillus nidulans. This systematic analysis will pave the way for future research into the complexity of the histone code and its functional implications on genome architecture and gene regulation in fungi.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Comparative Genomic Analyses of Cellulolytic Machinery Reveal Two Nutritional Strategies of Marine Labyrinthulomycetes Protists

Labyrinthulomycetes are a group of ubiquitous and diverse unicellular Stramenopiles and have long been known for their vital role in ocean carbon cycling. However, their ecological function from the perspective of organic matter degradation remains poorly understood. This study reports high-quality genomes of two newly isolated Labyrinthulomycetes strains, namely, Botryochytrium sp. strain S-28 and Oblongichytrium sp. strain S-429, and provides molecular analysis of their ecological functions using comparative genomics and a biochemical assay. Our results suggest that Labyrinthulomycetes may occupy multiple ecological niches in marine ecosystems because of the significant differences in gene function among different genera. Certain strains could degrade wheat bran independently by secreting cellulase. The key glycoside hydrolase families (GH1, GH5, and GH9) related to cellulase and the functional domains of carbohydrate-active enzymes (CAZymes) were more enriched in their genomes. This group can actively participate in marine biochemical cycles as decomposers. In contrast, other strains that could not produce cellulase may thrive as “leftover scavengers” and act as a source of nutrients to the higher-trophic-level plankton. In addition, our findings emphasize the dual roles of endoglucanase, acting as both exo- and endoglucanases, in the process of cellulose degradation. Using genomic, biochemical, and phylogenetic analyses, our study provides a broader insight into the nutritional patterns and ecological functions of Labyrinthulomycetes.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

Cave Thiovulum ( Candidatus Thiovulum stygium) differs metabolically and genomically from marine species

Thiovulum spp. (Campylobacterota) are large sulfur bacteria that form veil-like structures in aquatic environments. The sulfidic Movile Cave (Romania), sealed from the atmosphere for ~5 million years, has several aqueous chambers, some with low atmospheric O 2 (~7%). The cave’s surface-water microbial community is dominated by bacteria we identified as Thiovulum. We show that this strain, and others from subsurface environments, are phylogenetically distinct from marine Thiovulum. We assembled a closed genome of the Movile strain and confirmed its metabolism using RNAseq. We compared the genome of this strain and one we assembled from public data from the sulfidic Frasassi caves to four marine genomes, including Candidatus Thiovulum karukerense and Ca. T. imperiosus, whose genomes we sequenced. Despite great spatial and temporal separation, the genomes of the Movile and Frasassi Thiovulum were highly similar, differing greatly from the very diverse marine strains. We concluded that cave Thiovulum represent a new species, named here Candidatus Thiovulum stygium. Based on their genomes, cave Thiovulum can switch between aerobic and anaerobic sulfide oxidation using O 2 and NO 3 - as electron acceptors, the latter likely via dissimilatory nitrate reduction to ammonia. Thus, Thiovulum is likely important to both S and N cycles in sulfidic caves. Electron microscopy analysis suggests that at least some of the short peritrichous structures typical of Thiovulum are type IV pili, for which genes were found in all strains. These pili may play a role in veil formation, by connecting adjacent cells, and in the motility of these exceptionally fast swimmers.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Predicting Antimicrobial Resistance Using Partial Genome Alignments

Antimicrobial resistance (AMR) is an important global health threat that impacts millions of people worldwide each year. Developing methods that can detect and predict AMR phenotypes can help to mitigate the spread of AMR by informing clinical decision making and appropriate mitigation strategies. Many bioinformatic methods have been developed for predicting AMR phenotypes from whole-genome sequences and AMR genes, but recent studies have indicated that predictions can be made from incomplete genome sequence data. In order to more systematically understand this, we built random forest-based machine learning classifiers for predicting susceptible and resistant phenotypes for Klebsiella pneumoniae (1,640 strains), Mycobacterium tuberculosis (2,497 strains), and Salmonella enterica (1,981 strains). We started by building models from alignments that were based on a reference chromosome for each species. We then subsampled each chromosomal alignment and built models for the resulting subalignments, finding that very small regions, representing approximately 0.1 to 0.2% of the chromosome, are predictive. In K. pneumoniae, M. tuberculosis, and S. enterica, the subalignments are able to predict multiple AMR phenotypes with at least 70% accuracy, even though most do not encode an AMR-related function. We used these models to identify regions of the chromosome with high and low predictive signals. Finally, subalignments that retain high accuracy across larger phylogenetic distances were examined in greater detail, revealing genes and intergenic regions with potential links to AMR, virulence, transport, and survival under stress conditions. IMPORTANCE Antimicrobial resistance causes thousands of deaths annually worldwide. Understanding the regions of the genome that are involved in antimicrobial resistance is important for developing mitigation strategies and preventing transmission. Machine learning models are capable of predicting antimicrobial resistance phenotypes from bacterial genome sequence data by identifying resistance genes, mutations, and other correlated features. They are also capable of implicating regions of the genome that have not been previously characterized as being involved in resistance. In this study, we generated global chromosomal alignments for Klebsiella pneumoniae, Mycobacterium tuberculosis, and Salmonella enterica and systematically searched them for small conserved regions of the genome that enable the prediction of antimicrobial resistance phenotypes. In addition to known antimicrobial resistance genes, this analysis identified genes involved in virulence and transport functions, as well as many genes with no previous implication in antimicrobial resistance.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

A Meta-Analysis of the Protein Components in Rattlesnake Venom

The specificity and potency of venom components give them a unique advantage in developing various pharmaceutical drugs. Though venom is a cocktail of proteins, rarely are the synergy and association between various venom components studied. Understanding the relationship between various components of venom is critical in medical research. Using meta-analysis, we observed underlying patterns and associations in the appearance of the toxin families. For Crotalus, Dis has the most associations with the following toxins: PDE; BPP; CRL; CRiSP; LAAO; SVMP P-I and LAAO; SVMP P-III and LAAO. In Sistrurus venom, CTL and NGF have the most associations. These associations can predict the presence of proteins in novel venom and understand synergies between venom components for enhanced bioactivity. Using this approach, the need to revisit the classification of proteins as major components or minor components is highlighted. The revised classification of venom components is based on ubiquity, bioactivity, the number of associations, and synergies. The revised classification can be expected to trigger increased research on venom components, such as NGF, which have high biomedical significance. Using hierarchical clustering, we observed that the genera’s venom compositions were similar, based on functional characteristics rather than phylogenetic relationships.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2020

Laboratory colonization by Dirofilaria immitis alters the microbiome of female Aedes aegypti mosquitoes

Background: The ability of blood-feeding arthropods to successfully acquire and transmit pathogens of medical and veterinary importance has been shown to be interfered with, or enhanced by, the arthropod’s native microbiome. Mosquitoes transmit viruses, protozoan and filarial nematodes, the majority of which contribute to the 17% of infectious disease cases worldwide. Diroflaria immitis, a mosquito-transmitted filarial nematodes of dogs and cats, is vectored by several mosquito species including Aedes aegypti. Methods: In this study, we investigated the impact of D. immitis colonization on the microbiome of laboratory reared female Ae. aegypti. Metagenomic analysis of the V3–V4 variable region of the microbial 16S RNA gene was used for identification of the microbial differences down to species level. Results: We generated a total of 1068 OTUs representing 16 phyla, 181 genera and 271 bacterial species. Overall, in order of abundance, Proteobacteria, Bacteroidetes, Actinobacteria and Firmicutes were the most represented phylum with D. immitis-infected mosquitoes having more of Proteobacteria (71%) than uninfected mosquitoes (56.9%). An interesting finding in this study is the detection of Klebsiella oxytoca in relatively similar abundance in infected and uninfected mosquitoes, suggesting a possible endosymbiotic relationship, and has been previously shown to indirectly compete for nutrients with fungi on domestic housefly eggs and larvae. While D. immitis colonization has no effect on the overall species richness, we identified significant differences in the composition of selected bacterial genera and phyla between the two groups. We also reported distinct compositional and phylogenetic differences in the individual bacterial species when commonly identified bacteria were compared. Conclusions: To the best of our knowledge, this is the first study to understand the impact of a filarial infection on the microbiome of its mosquito vector. Further studies are required to identify bacteria species that could play an important role in the mosquito biology. While the microbiome composition of Ae. aegypti mosquito have been previously reported, our study shows that in an effort to establish itself, a filarial nematode modifies and alters the overall microbial diversity within its mosquito host.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2020

Disentangling Sources of Gene Tree Discordance in Phylogenomic Data Sets: Testing Ancient Hybridizations in Amaranthaceae s.l

Gene tree discordance in large genomic data sets can be caused by evolutionary processes such as incomplete lineage sorting and hybridization, as well as model violation, and errors in data processing, orthology inference, and gene tree estimation. Species tree methods that identify and accommodate all sources of conflict are not available, but a combination of multiple approaches can help tease apart alternative sources of conflict. Here, using a phylotranscriptomic analysis in combination with reference genomes, we test a hypothesis of ancient hybridization events within the plant family Amaranthaceae s.l. that was previously supported by morphological, ecological, and Sanger-based molecular data. The data set included seven genomes and 88 transcriptomes, 17 generated for this study. We examined gene-tree discordance using coalescent-based species trees and network inference, gene tree discordance analyses, site pattern tests of introgression, topology tests, synteny analyses, and simulations. We found that a combination of processes might have generated the high levels of gene tree discordance in the backbone of Amaranthaceae s.l. Furthermore, we found evidence that three consecutive short internal branches produce anomalous trees contributing to the discordance. Overall, our results suggest that Amaranthaceae s.l. might be a product of an ancient and rapid lineage diversification, and remains, and probably will remain, unresolved. This work highlights the potential problems of identifiability associated with the sources of gene tree discordance including, in particular, phylogenetic network methods. Our results also demonstrate the importance of thoroughly testing for multiple sources of conflict in phylogenomic analyses, especially in the context of ancient, rapid radiations. We provide several recommendations for exploring conflicting signals in such situations.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

To date, little is known about the evolution of fern genomes, with only two small genomes published from the heterosporous Salviniales. Here we assembled the genome of Alsophila spinulosa, known as the flying spider-monkey tree fern, onto 69 pseudochromosomes. The remarkable preservation of synteny, despite resulting from an ancient whole-genome duplication over 100 million years ago, is unprecedented in plants and probably speaks to the uniqueness of tree ferns. Our detailed investigations into stem anatomy and lignin biosynthesis shed new light on the evolution of stem formation in tree ferns. We identified a phenolic compound, alsophilin, that is abundant in xylem, and we provided the molecular basis for its biosynthesis. Finally, analysis of demographic history revealed two genetic bottlenecks, resulting in rapid demographic declines of A. spinulosa. The A. spinulosa genome fills a crucial gap in the plant genomic landscape and helps elucidate many unique aspects of tree fern biology.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Antimicrobial resistance and genomic characterization of Salmonella Dublin isolates in cattle from the United States

Salmonella enterica subspecies enterica serotype Dublin is a host-adapted serotype in cattle, associated with enteritis and systemic disease. The primary clinical manifestation of Salmonella Dublin infection in cattle, especially calves, is respiratory disease. While rare in humans, it can cause severe illness, including bacteremia, with hospitalization and death. In the United States, S . Dublin has become one of the most multidrug-resistant serotypes. The objective of this study was to characterize S . Dublin isolates from sick cattle by analyzing phenotypic and genotypic antimicrobial resistance (AMR) profiles, the presence of plasmids, and phylogenetic relationships. S . Dublin isolates (n = 140) were selected from submissions to the NVSL for Salmonella serotyping (2014–2017) from 21 states. Isolates were tested for susceptibility against 14 class-representative antimicrobial drugs. Resistance profiles were determined using the ABRicate with Resfinder and NCBI databases, AMRFinder and PointFinder. Plasmids were detected using ABRicate with PlasmidFinder. Phylogeny was determined using vSNP. We found 98% of the isolates were resistant to more than 4 antimicrobials. Only 1 isolate was pan-susceptible and had no predicted AMR genes. All S . Dublin isolates were susceptible to azithromycin and meropenem. They showed 96% resistance to sulfonamides, 97% to tetracyclines, 95% to aminoglycosides and 85% to beta-lactams. The most common AMR genes were: sulf2 and tetA (98.6%), aph(6)-Id (97.9%), aph(3’’)-Ib, (97.1%), floR (94.3%), and blaCMY-2 (85.7%). All quinolone resistant isolates presented mutations in gyr A. Ten plasmid types were identified among all isolates with IncA/C2, IncX1, and IncFII(S) being the most frequent. The S . Dublin isolates show low genomic genetic diversity. This study provided antimicrobial susceptibility and genomic insight into S . Dublin clinical isolates from cattle in the U.S. Further sequence analysis integrating food and human origin S . Dublin isolates may provide valuable insight on increased virulence observed in humans.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2024

Alkaloids are associated with increased microbial diversity and metabolic function in poison frogs

Shifts in host-associated microbiomes can impact both host and microbes. It is of interest to understand how perturbations, like the introduction of exogenous chemicals, impact microbiomes. In poison frogs (family Dendrobatidae), the skin microbiome is exposed to alkaloids that the frogs sequester for defense. These alkaloids are antimicrobial; however, their effect on the frogs’ skin microbiome is unknown. To test this, we characterized microbial communities from field-collected dendrobatid frogs. Then, we conducted a laboratory experiment to monitor the effect of the alkaloid decahydroquinoline (DHQ) on the microbiome of two frog species with contrasting alkaloid loads in nature. In both datasets, we found that alkaloid-exposed microbiomes were more phylogenetically diverse, with an increase in diversity among rare taxa. Further, to better understand the isolate-specific response to alkaloids, we cultured microbial isolates from poison frog skin and found that many isolates exhibited enhanced growth or were not impacted by the addition of DHQ. To further explore the microbial response to alkaloids, we sequenced the metagenomes from high- and low-alkaloid frogs and observed a greater diversity of genes associated with nitrogen and carbon metabolism in high-alkaloid frogs. From these data, we hypothesized that some strains may metabolize the alkaloids. We used stable isotope tracing coupled to nanoSIMS (nanoscale secondary ion mass spectrometry), which supported the idea that some of these isolates are able to metabolize DHQ. Together, these data suggest that poison frog alkaloids open new niches for skin-associated microbes with specific adaptations, such as alkaloid metabolism, that enable survival in this environment.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Phylogenetically diverse wild plant species use common biochemical strategies to thrive in the Atacama Desert

The best ideotypes are under mounting pressure due to increased aridity. Understanding the conserved molecular mechanisms that evolve in wild plants adapted to harsh environments is crucial in developing new strategies for agriculture. Yet our knowledge of such mechanisms in wild species is scant. We performed metabolic pathway reconstruction using transcriptome information from 32 Atacama and phylogenetically related species that do not live in Atacama (sister species). We analyzed reaction enrichment to understand the commonalities and differences of Atacama plants. To gain insights into the mechanisms that ensure survival, we compared expressed gene isoform numbers and gene expression patterns between the annotated biochemical reactions from 32 Atacama and sister species. We found biochemical convergences characterized by reactions enriched in at least 50% of the Atacama species, pointing to potential advantages against drought and nitrogen starvation, for instance. Furthermore, these findings suggest that the adaptation in the Atacama Desert may result in part from shared genetic legacies governing the expression of key metabolic pathways to face harsh conditions. Enriched reactions corresponded to ubiquitous compounds common to extreme and agronomic species and were congruent with our previous metabolomic analyses. Convergent adaptive traits offer promising candidates for improving abiotic stress resilience in crop species.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Bacterial Origin and Reductive Evolution of the CPR Group

The candidate phyla radiation (CPR) is a proposed subdivision within the bacterial domain comprising several candidate phyla. CPR organisms are united by small genome and physical sizes, lack several metabolic enzymes, and populate deep branches within the bacterial subtree of life. Here, these features raise intriguing questions regarding their origin and mode of evolution. In this study, we performed a comparative and phylogenomic analysis to investigate CPR origin and evolution. Unlike previous gene/protein sequence-based reports of CPR evolution, we used protein domain superfamilies classified by protein structure databases to resolve the evolutionary relationships of CPR with non-CPR bacteria, Archaea, Eukarya, and viruses. Across all supergroups, CPR shared maximum superfamilies with non-CPR bacteria and were placed as deep branching bacteria in most phylogenomic trees. CPR contributed 1.22% of new superfamilies to bacteria including the ribosomal protein L19e and encoded four core superfamilies that are likely involved in cell-to-cell interaction and establishing episymbiotic lifestyles. Although CPR and non-CPR bacterial proteomes gained common superfamilies over the course of evolution, CPR and Archaea had more common losses. These losses mostly involved metabolic superfamilies. In fact, phylogenies built from only metabolic protein superfamilies separated CPR and non-CPR bacteria. These findings indicate that CPR are bacterial organisms that have probably evolved in an Archaea-like manner via the early loss of metabolic functions. We also discovered that phylogenies built from metabolic and informational superfamilies gave contrasting views of the groupings among Archaea, Bacteria, and Eukarya, which add to the current debate on the evolutionary relationships among superkingdoms.

59 BASIC BIOLOGICAL SCIENCES↗