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DOE OSTI2020

Metabolic Feedback Inhibition Influences Metabolite Secretion by the Human Gut Symbiont Bacteroides thetaiotaomicron

ABSTRACT Microbial metabolism and trophic interactions between microbes give rise to complex multispecies communities in microbe-host systems. Bacteroides thetaiotaomicron ( B. theta ) is a human gut symbiont thought to play an important role in maintaining host health. Untargeted nuclear magnetic resonance metabolomics revealed B. theta secretes specific organic acids and amino acids in defined minimal medium. Physiological concentrations of acetate and formate found in the human intestinal tract were shown to cause dose-dependent changes in secretion of metabolites known to play roles in host nutrition and pathogenesis. While secretion fluxes varied, biomass yield was unchanged, suggesting feedback inhibition does not affect metabolic bioenergetics but instead redirects carbon and energy to CO 2 and H 2 . Flux balance analysis modeling showed increased flux through CO 2 -producing reactions under glucose-limiting growth conditions. The metabolic dynamics observed for B. theta , a keystone symbiont organism, underscores the need for metabolic modeling to complement genomic predictions of microbial metabolism to infer mechanisms of microbe-microbe and microbe-host interactions. IMPORTANCE Bacteroides is a highly abundant taxon in the human gut, and Bacteroides thetaiotaomicron ( B. theta ) is a ubiquitous human symbiont that colonizes the host early in development and persists throughout its life span. The phenotypic plasticity of keystone organisms such as B. theta is important to understand in order to predict phenotype(s) and metabolic interactions under changing nutrient conditions such as those that occur in complex gut communities. Our study shows B. theta prioritizes energy conservation and suppresses secretion of “overflow metabolites” such as organic acids and amino acids when concentrations of acetate are high. Secreted metabolites, especially amino acids, can be a source of nutrients or signals for the host or other microbes in the community. Our study suggests that when metabolically stressed by acetate, B. theta stops sharing with its ecological partners.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

A Genome-Scale Metabolic Model of Anabaena 33047 to Guide Genetic Modifications to Overproduce Nylon Monomers

Nitrogen fixing-cyanobacteria can significantly improve the economic feasibility of cyanobacterial production processes by eliminating the requirement for reduced nitrogen. Anabaena sp. ATCC 33047 is a marine, heterocyst forming, nitrogen fixing cyanobacteria with a very short doubling time of 3.8 h. We developed a comprehensive genome-scale metabolic (GSM) model, iAnC892, for this organism using annotations and content obtained from multiple databases. iAnC892 describes both the vegetative and heterocyst cell types found in the filaments of Anabaena sp. ATCC 33047. iAnC892 includes 953 unique reactions and accounts for the annotation of 892 genes. Comparison of iAnC892 reaction content with the GSM of Anabaena sp. PCC 7120 revealed that there are 109 reactions including uptake hydrogenase, pyruvate decarboxylase, and pyruvate-formate lyase unique to iAnC892. iAnC892 enabled the analysis of energy production pathways in the heterocyst by allowing the cell specific deactivation of light dependent electron transport chain and glucose-6-phosphate metabolizing pathways. The analysis revealed the importance of light dependent electron transport in generating ATP and NADPH at the required ratio for optimal N2 fixation. When used alongside the strain design algorithm, OptForce, iAnC892 recapitulated several of the experimentally successful genetic intervention strategies that over produced valerolactam and caprolactam precursors.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

maslov-group/FUN-PROSE

mRNA levels of all genes in a genome is a critical piece of information defining the overall state of the cell in a given environmental condition. Being able to reconstruct such condition-specific expression in fungal genomes is particularly important to metabolically engineer these organisms to produce desired chemicals in industrially scalable conditions. Most previous deep learning approaches focused on predicting the average expression levels of a gene based on its promoter sequence, ignoring its variation across different conditions. Here we present FUN-PROSE—a deep learning model trained to predict differential expression of individual genes across various conditions using their promoter sequences and expression levels of all transcription factors. We train and test our model on three fungal species and get the correlation between predicted and observed condition-specific gene expression as high as 0.85. We then interpret our model to extract promoter sequence motifs responsible for variable expression of individual genes. We also carried out input feature importance analysis to connect individual transcription factors to their gene targets. A sizeable fraction of both sequence motifs and TF-gene interactions learned by our model agree with previously known biological information, while the rest corresponds to either novel biological facts or indirect correlations.

Liu, Simon↗

DOE OSTI2025

Stage-resolved gene regulatory network analysis reveals developmental reprogramming and genes with robust stem-preferred expression in sorghum

Sorghum bicolor is a deep-rooted, heat- and drought-tolerant crop that thrives on marginal lands and is increasingly valued for its applications in biofuel, bioenergy, and biopolymer production. The sorghum stem, which can reach 4–5 m in length, serves as the primary reservoir of both lignocellulosic biomass and soluble sugars, making it a promising bioenergy feedstock. Although recent advances in genetic, genomic, and transcriptomic resources have improved our understanding of sorghum biology, comprehensive genome-wide analyses of functional dynamics across diverse organ types and developmental stages remain limited. In particular, candidate genes with stem preferred expression pattern or their associated cis-regulatory elements, which may program key stem-related functions and enable organ- or tissue-specific engineering, have not yet been identified.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

FUN-PROSE: A deep learning approach to predict condition-specific gene expression in fungi

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Generating Co-expression Networks for Three Cyanobacteria: Synechococcus sp. PCC 7942, Synechococcus sp. PCC 7002, Synechocystis sp. PCC 6803

Cyanobacteria are photosynthetic organisms capable of high growth rate and represent a promising bioplatform for harnessing the sun’s energy to make biofuel. Additionally, the process of photosynthesis absorbs CO2 from the environment. Understanding the metabolic processes involved in photosynthesis could lead to solutions to the recent rise of CO2 concentration in Earth’s atmosphere and the associated climate change. More research on the transcriptional regulation of these cells is needed to learn how to harness the untapped potential of cyanobacteria for these applications. Transcriptional analysis via RNA-seq provides an understanding of how gene expression changes at the mRNA level under diverse growing conditions. I systematically collected and analyzed RNA-Seq data obtained under a variety of conditions and available on the NCBI database for three cyanobacteria model organisms: Synechococcus elongatus sp. PCC 7942, Synechococcus sp. PCC 7002, and Synechocystis sp. PCC 6803. For each organism, the data was mapped to a reference genome to characterize the RNA expression profile. Samples were checked for quality based on the number of reads and the correlation of the expression profile between labeled replicates. All samples were transformed into transcripts per million reads, followed by a log transformation to account for the wide range of sample sizes. Gene co-expression networks were generated and analyzed for each species using Cytoscape. These networks provide a base level of gene expression for each species. The network topology and high-betweeness nodes of these networks need to be analyzed further to provide insight on potential ways to harness cyanobacteria genetics. Additionally, these datasets can be used together to form a core genome network analysis- one that includes only the genes that are homologous between the three species. This project has prepared the way for a more in-depth study on photosynthetic microbes on a genetic level.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Antarctic lake viromes reveal potential virus associated influences on nutrient cycling in ice-covered lakes

The McMurdo Dry Valleys (MDVs) of Antarctica are a mosaic of extreme habitats which are dominated by microbial life. The MDVs include glacial melt holes, streams, lakes, and soils, which are interconnected through the transfer of energy and flux of inorganic and organic material via wind and hydrology. For the first time, we provide new data on the viral community structure and function in the MDVs through metagenomics of the planktonic and benthic mat communities of Lakes Bonney and Fryxell. Viral taxonomic diversity was compared across lakes and ecological function was investigated by characterizing auxiliary metabolic genes (AMGs) and predicting viral hosts. Our data suggest that viral communities differed between the lakes and among sites: these differences were connected to microbial host communities. AMGs were associated with the potential augmentation of multiple biogeochemical processes in host, most notably with phosphorus acquisition, organic nitrogen acquisition, sulfur oxidation, and photosynthesis. Viral genome abundances containing AMGs differed between the lakes and microbial mats, indicating site specialization. Using procrustes analysis, we also identified significant coupling between viral and bacterial communities (p = 0.001). Finally, host predictions indicate viral host preference among the assembled viromes. Collectively, our data show that: (i) viruses are uniquely distributed through the McMurdo Dry Valley lakes, (ii) their AMGs can contribute to overcoming host nutrient limitation and, (iii) viral and bacterial MDV communities are tightly coupled.

Microbiology↗

NASA NTRS2004

Deuterostome Evolution: Large Data Set Analysis

This award allowed us to develop novel hardware for phylogenetics, collect genomic data and produce several phylogenies of deuterostome organisms, communicate the results publicly, release software into the public domain, publish textbooks and papers, and prepare for the next research projects. There are no resulting subject inventions to report. We review these activities in three sections: 1) Hardware and software and development; 2) Evolutionary biology research; 3) Our proposed future direction, predictive analysis of pathogens in support of the NASA mission.

Janies, Daniel↗

NASA NTRS2014

A ribozyme that triphosphorylates RNA 50-hydroxyl groups

The RNA world hypothesis describes a stage in the early evolution of life in which RNA served as genome and as the only genome-encoded catalyst. To test whether RNA world organisms could have used cyclic trimetaphosphate as an energy source, we developed an in vitro selection strategy for isolating ribozymes that catalyze the triphosphorylation of RNA 50 -hydroxyl groups with trimetaphosphate. Several active sequences were isolated, and one ribozyme was analyzed in more detail. The ribozyme was truncated to 96 nt, while retaining full activity. It was converted to a transformat and reacted with rates of 0.16 min1 under optimal conditions. The secondary structure appears to contain a four-helical junction motif. This study showed that ribozymes can use trimetaphosphate to triphosphorylate RNA 50 -hydroxyl groups and suggested that RNA world organisms could have used trimetaphosphate as their energy source.

Janina E. Moretti↗

NASA NTRS2001

Analysis of the myosins encoded in the recently completed Arabidopsis thaliana genome sequence

BACKGROUND: Three types of molecular motors play an important role in the organization, dynamics and transport processes associated with the cytoskeleton. The myosin family of molecular motors move cargo on actin filaments, whereas kinesin and dynein motors move cargo along microtubules. These motors have been highly characterized in non-plant systems and information is becoming available about plant motors. The actin cytoskeleton in plants has been shown to be involved in processes such as transportation, signaling, cell division, cytoplasmic streaming and morphogenesis. The role of myosin in these processes has been established in a few cases but many questions remain to be answered about the number, types and roles of myosins in plants. RESULTS: Using the motor domain of an Arabidopsis myosin we identified 17 myosin sequences in the Arabidopsis genome. Phylogenetic analysis of the Arabidopsis myosins with non-plant and plant myosins revealed that all the Arabidopsis myosins and other plant myosins fall into two groups - class VIII and class XI. These groups contain exclusively plant or algal myosins with no animal or fungal myosins. Exon/intron data suggest that the myosins are highly conserved and that some may be a result of gene duplication. CONCLUSIONS: Plant myosins are unlike myosins from any other organisms except algae. As a percentage of the total gene number, the number of myosins is small overall in Arabidopsis compared with the other sequenced eukaryotic genomes. There are, however, a large number of class XI myosins. The function of each myosin has yet to be determined.

NASA Discipline Plant Biology↗

DOE OSTI2025

The architecture of resilience: a genome assembly of Myrothamnus flabellifolia sheds light on desiccation tolerance and sex determination

Myrothamnus flabellifolia is a dioecious resurrection plant endemic to southern Africa that has become an important model for understanding desiccation tolerance. Despite its ecological and medicinal significance, genomic and transcriptomic resources for the species are limited. We generated a chromosome-level, haplotype-resolved reference genome assembly and annotation for M. flabellifolia and conducted transcriptomic profiling across a natural dehydration–rehydration time course in the field. Genome architecture and sex determination were characterized, and co-expression network and cis-regulatory element (CRE) enrichment analyses were used to investigate dynamic responses to desiccation. The 1.28-Gb genome exhibits unusually consistent chromatin architecture with unique chromosome organization across highly divergent haplotypes. We identified an XY sexual system with a small sex-determining region on Chromosome 8. Transcriptomic responses varied with dehydration severity, pointing to early suppression of growth, progressive activation of protective mechanisms, and subsequent return to homeostasis upon rehydration. Late embryogenesis abundant and early light-induced protein transcripts were dynamically regulated and showed enrichment of abscisic acid and stress-responsive CREs pointing toward conserved responses. Together, this study provides foundational resources for understanding the genomic architecture and reproductive biology of M. flabellifolia and offers new insights into the mechanisms of desiccation tolerance.

chromosome structure↗

NASA NTRS2018

GeneLab: Omics Database for Spaceflight Experiments

Motivation - To curate and organize expensive spaceflight experiments conducted aboard space stations and maximize the scientific return of investment, while democratizing access to vast amounts of spaceflight related omics data generated from several model organisms. Results - The GeneLab Data System (GLDS) is an open access database containing fully coordinated and curated "omics" (genomics, transcriptomics, proteomics, metabolomics) data, detailed metadata and radiation dosimetry for a variety of model organisms. GLDS is supported by an integrated data system allowing federated search across several public bioinformatics repositories. Archived datasets can be queried using full-text search (e.g., keywords, Boolean and wildcards) and results can be sorted in multifactorial manner using assistive filters. GLDS also provides a collaborative platform built on GenomeSpace for sharing files and analyses with collaborators. It currently houses 172 datasets and supports standard guidelines for submission of datasets, MIAME (for microarray), ENCODE Consortium Guidelines (for RNA-seq) and MIAPE Guidelines (for proteomics).

omics↗

NASA NTRS2005

Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes

The important role that cilia and flagella play in human disease creates an urgent need to identify genes involved in ciliary assembly and function. The strong and specific induction of flagellar-coding genes during flagellar regeneration in Chlamydomonas reinhardtii suggests that transcriptional profiling of such cells would reveal new flagella-related genes. We have conducted a genome-wide analysis of RNA transcript levels during flagellar regeneration in Chlamydomonas by using maskless photolithography method-produced DNA oligonucleotide microarrays with unique probe sequences for all exons of the 19,803 predicted genes. This analysis represents previously uncharacterized whole-genome transcriptional activity profiling study in this important model organism. Analysis of strongly induced genes reveals a large set of known flagellar components and also identifies a number of important disease-related proteins as being involved with cilia and flagella, including the zebrafish polycystic kidney genes Qilin, Reptin, and Pontin, as well as the testis-expressed tubby-like protein TULP2.

Polycystic Kidney Diseases/genetics↗

DOE OSTI2020

Comparative Genomic Analysis of Ochratoxin A Biosynthetic Cluster in Producing Fungi: New Evidence of a Cyclase Gene Involvement

The widespread use of Next-Generation Sequencing has opened a new era in the study of biological systems by significantly increasing the catalog of fungal genomes sequences and identifying gene clusters for known secondary metabolites as well as novel cryptic ones. However, most of these clusters still need to be examined in detail to completely understand the pathway steps and the regulation of the biosynthesis of metabolites. Genome sequencing approach led to the identification of the biosynthetic genes cluster of ochratoxin A (OTA) in a number of producing fungal species. Ochratoxin A is a potent pentaketide nephrotoxin produced by Aspergillus and Penicillium species and found as widely contaminant in food, beverages and feed. The increasing availability of several new genome sequences of OTA producer species in JGI Mycocosm and/or GenBank databanks led us to analyze and update the gene cluster structure in 19 Aspergillus and 2 Penicillium OTA producing species, resulting in a well conserved organization of OTA core genes among the species. Furthermore, our comparative genome analyses evidenced the presence of an additional gene, previously undescribed, located between the polyketide and non-ribosomal synthase genes in the cluster of all the species analyzed. The presence of a SnoaL cyclase domain in the sequence of this gene supports its putative role in the polyketide cyclization reaction during the initial steps of the OTA biosynthesis pathway. The phylogenetic analysis showed a clustering of OTA SnoaL domains in accordance with the phylogeny of OTA producing species at species and section levels. The characterization of this new OTA gene, its putative role and its expression evidence in three important representative producing species, are reported here for the first time.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

Novel anaerobic selenium oxyanion reducers native to FGD wastewater for enhanced selenium removal

Biological treatment is a recognized approach for removing selenate and selenite oxyanions present in flue gas desulfurization (FGD) wastewater. However, the knowledge of the specific microbial species or communities responsible for reducing water-soluble selenium oxyanions to insoluble elemental selenium remains limited. In addition, the selenium oxyanion reduction genes and pathways have yet to be understood in these wastewaters. This study characterizes selenium oxyanion-reducing bacteria (SeRB) native to FGD wastewater, and the resulting elemental selenium particles formed. By selecting native SeRB microbes in a defined media, a novel resolution of these organisms has been achieved. This research identifies previously unrecognized selenium oxyanion-reducing capabilities in Anaerosolibacter, alongside predominant SeRB from Mesobacillus and Tepidibacillus genera. This work encompasses both 16S and metagenomic techniques to recover novel metagenome-assembled genomes, distinct to this environment. The biogenic selenium produced by these organisms was predominantly of elemental selenium, either amorphous or with a hexagonal structure. This study identifies the SeRB present in FGD wastewater and characterizes their selenium products, offering crucial insights to enhance the efficiency of biological treatment strategies and the potential of selenium recovery from this industrial waste.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS1999

An Inherited Efficiencies Model of Non-Genomic Evolution

A model for the evolution of biological systems in the absence of a nucleic acid-like genome is proposed and applied to model the earliest living organisms -- protocells composed of membrane encapsulated peptides. Assuming that the peptides can make and break bonds between amino acids, and bonds in non-functional peptides are more likely to be destroyed than in functional peptides, it is demonstrated that the catalytic capabilities of the system as a whole can increase. This increase is defined to be non-genomic evolution. The relationship between the proposed mechanism for evolution and recent experiments on self-replicating peptides is discussed.

New, Michael H.↗

DOE OSTI2024

Commentary: Duckweeds as model organisms for metabolic studies

Duckweeds have many practical applications, for example in human nutrition, as animal feed, in the production of bioplastics or vaccines, and phytoremediation (Acosta et al., 2021). Under most conditions, they reproduce asexually which provides genetically uniform material with predictable patterns of growth that make them ideal as sentinel organisms for phytotoxicity testing (Park et al., 2021). Asexual growth also results in high biomass production which makes duckweeds promising candidates as biofuel feedstocks (Acosta et al., 2021; Liang et al., 2023). In addition, duckweed species like Lemna minor and Spirodela polyrhiza are also reemerging as model organisms in plant biology as high-quality full genome assemblies and other genomic resources become available (Chang et al., 2016; Acosta et al., 2021). We argue that duckweed species are particularly of interest for the study of primary plant metabolism. Primary metabolism concerns the part of metabolism that is directly involved in the growth and development of plants, and which tends to be highly conserved among plant species. What makes duckweeds particularly attractive is that when grown on liquid media more precise control of physiological conditions can be attained relative to growth of plants in soil. Also, due to their relatively simple anatomical structure and asexual reproduction of fronds by budding, precise characterization of the physiological state under study is possible through one simple metric, i.e., the specific growth rate (rate of dry weight increase per existing dry weight), which can be incorporated relatively easily into metabolic models. This is not possible for land plants, such as Arabidopsis, because over the course of their life cycle, they go through multiple growth stages and phases of anatomical differentiation, which are much more complex to quantify. Furthermore, duckweeds can grow on organic substrates under heterotrophic or photomixotrophic conditions that facilitate isotope tracer studies. For example, in a previous study on duckweed by one of the authors, Lemna gibba (L). was grown on glucose with a position-specific 13 C-label that can be detected and resolved by Mass Spectrometry or Nuclear Magnetic Resonance spectrometry. Using this approach, the 13 C-label was traced into biomass compounds formed from glucose, particularly isoprenoid compounds. Some of the resulting labeling patterns were in apparent disagreement with predictions based on known metabolic pathways for the biosynthesis of isopentenyl pyrophosphate, the universal building block for isoprenoids, (Lichtenthaler et al., 1997). From this data it was deduced that isoprenoid compounds such as carotenoids and isoprenoid chains of phytol and plastoquinone, synthesized in the chloroplast, are produced via a previously unreported plant metabolic pathway, now known as the methylerythitol/deoxyxylulose-5-phosphate pathway (Lichtenthaler et al., 1997).

59 BASIC BIOLOGICAL SCIENCES↗