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DOE OSTI2022

BETO 2021 Peer Review: Algae Biotechnology Partnership - Technology Area Session: Advanced Algae Systems

Development of advanced genetic and genomic tools for targeted algal metabolic engineering pursuits will be integral to achieving target biomass productivity and, ultimately, the BETO goal of cost-competitive biofuels derived from algal biomass by 2022. However, at present, broad-host-range tool development is currently hindered by strain-specific negative regulatory mechanisms. Indeed, the biological processes controlling algal transcription and translation are subject to complex host regulation, which often presents hurdles for targeted genetic engineering strategies. Advanced genetic approaches offer a means to rewire these regulatory systems and/or introduce novel functionality into algal biocatalysts. Synthetic systems biology approaches also present a means to construct novel genetic regulatory networks and rewire natural biological systems to establish an “orthogonal central dogma,” wherein non-native control elements are introduced into or evolved in host microbes for bypass of host control. To this end, the Algae Biotechnology Partnership aims to develop advanced genetic editing tools and synthetic and orthogonal genetic regulatory systems to enable universal metabolic engineering strategies in top-candidate deployment algal strains. Successful development will ultimately open the door for targeted strain-engineering strategies, aimed at maximizing algal outdoor biomass production, composition, and strain robustness.

biocatalysis↗

DOE OSTI2026

Ancient co-option of LTR retrotransposons as yeast centromeres

Centromeres ensure accurate chromosome segregation, yet their DNA evolves rapidly across eukaryotes leaving the origins of new centromere architectures unclear. The brewer’s yeast Saccharomyces cerevisiae exemplifies this long-standing puzzle. Its centromeres shifted ancestrally from large, repeat-rich, epigenetically specified forms to the compact, genetically defined ‘point’ centromeres. How this transition occurred has remained unresolved6. Here we identify evolutionarily related ‘proto-point’ centromeres that provide a resolution to the evolutionary origins of point centromeres. Proto-point centromeres contain a single centromeric nucleosome positioned over an AT-rich core, accompanied by relaxed organization and sequence variability of flanking cis-elements. In two species, these proto-point centromeres lie within retrotransposon-derived repeat clusters, linking ancestral repeat-rich centromeres to genetically encoded ones. Comparative and phylogenetic analyses indicate that proto-point and point centromeres evolved in an ancestor with retrotransposon-rich centromeres. These results identify long-terminal-repeat retrotransposons, specifically Ty5 sequences, as the genetic substrate for point-centromere evolution and provide a mechanistic route by which an epigenetic centromere can become genetically specified. More broadly, they show how selfish elements can be co-opted to perform essential chromosomal functions.

Haase, Max A. B. [Max Planck Institute of Molecula↗

NASA NTRS2009

Chemistry of Diogenites and Evolution of their Parent Asteroid

Diogenites are orthopyroxenite meteorites [1]. Most are breccias, but remnant textures indicate they were originally coarse-grained rocks, with grain sizes of order of cm. Their petrography, and major and trace element chemistry support an origin as crustal cumulates from a differentiated asteroid. Diogenites are genetically related to the basaltic and cumulate-gabbro eucrites, and the polymict breccias known as howardites, collectively, the HED suite. Spectroscopic observations, orbit data and dynamical arguments strongly support the hypothesis that asteroid 4 Vesta is the parent object for HED meteorites [2]. Here we discuss our new trace element data for a suite of diogenites and integrate these into the body of literature data. We use the combined data set to discuss the petrologic evolution of diogenites and 4 Vesta.

Mittlefehldt, D.W.↗

DOE OSTI2024

Enhancing Thomson scattering polychromator performance with multi-pass spectral filters

In photon-deficient, noncollective Thomson scattering diagnostics, filter polychromators are typically employed in the spectral analysis of Thomson-scattered signals to achieve acceptable signal-to-noise performance. Currently, the most common polychromator filter configuration employs a set of single-passband optical filters that define individual spectral channels. Here, we introduce a new spectral analysis method for Thomson scattering based on spectral filters with multiple passbands, referred to as Thomson scattering spectral multiplexing. Implementing multi-bandpass spectral filters on polychromators increases the achievable range of electron temperature measurement for a given number of filters employed. In addition, Thomson scattering spectral multiplexing reduces systematic measurement uncertainty, with fewer required spectral channels, thereby decreasing light loss from reduced optical element interactions. A multi-bandpass filter set, optimized by a genetic algorithm, has been successfully installed and tested on the Helically Symmetric eXperiment (HSX), demonstrating the benefits of the Thomson scattering spectral multiplexing method.

Instruments & Instrumentation↗

DOE OSTI2022

The tRNA discriminator base defines the mutual orthogonality of two distinct pyrrolysyl-tRNA synthetase/tRNAPyl pairs in the same organism

Abstract Site-specific incorporation of distinct non-canonical amino acids into proteins via genetic code expansion requires mutually orthogonal aminoacyl-tRNA synthetase/tRNA pairs. Pyrrolysyl-tRNA synthetase (PylRS)/tRNAPyl pairs are ideal for genetic code expansion and have been extensively engineered for developing mutually orthogonal pairs. Here, we identify two novel wild-type PylRS/tRNAPyl pairs simultaneously present in the deep-rooted extremely halophilic euryarchaeal methanogen Candidatus Methanohalarchaeum thermophilum HMET1, and show that both pairs are functional in the model halophilic archaeon Haloferax volcanii. These pairs consist of two different PylRS enzymes and two distinct tRNAs with dissimilar discriminator bases. Surprisingly, these two PylRS/tRNAPyl pairs display mutual orthogonality enabled by two unique features, the A73 discriminator base of tRNAPyl2 and a shorter motif 2 loop in PylRS2. In vivo translation experiments show that tRNAPyl2 charging by PylRS2 is defined by the enzyme's shortened motif 2 loop. Finally, we demonstrate that the two HMET1 PylRS/tRNAPyl pairs can simultaneously decode UAG and UAA codons for incorporation of two distinct noncanonical amino acids into protein. This example of a single base change in a tRNA leading to additional coding capacity suggests that the growth of the genetic code is not yet limited by the number of identity elements fitting into the tRNA structure.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Coding and noncoding variants in EBF3 are involved in HADDS and simplex autism

Abstract Background Previous research in autism and other neurodevelopmental disorders (NDDs) has indicated an important contribution of protein-coding (coding) de novo variants (DNVs) within specific genes. The role of de novo noncoding variation has been observable as a general increase in genetic burden but has yet to be resolved to individual functional elements. In this study, we assessed whole-genome sequencing data in 2671 families with autism (discovery cohort of 516 families, replication cohort of 2155 families). We focused on DNVs in enhancers with characterized in vivo activity in the brain and identified an excess of DNVs in an enhancer named hs737. Results We adapted the fitDNM statistical model to work in noncoding regions and tested enhancers for excess of DNVs in families with autism. We found only one enhancer (hs737) with nominal significance in the discovery (p = 0.0172), replication (p = 2.5 × 10 −3 ), and combined dataset (p = 1.1 × 10 −4 ). Each individual with a DNV in hs737 had shared phenotypes including being male, intact cognitive function, and hypotonia or motor delay. Our in vitro assessment of the DNVs showed they all reduce enhancer activity in a neuronal cell line. By epigenomic analyses, we found that hs737 is brain-specific and targets the transcription factor gene EBF3 in human fetal brain. EBF3 is genome-wide significant for coding DNVs in NDDs (missense p = 8.12 × 10 −35 , loss-of-function p = 2.26 × 10 −13 ) and is widely expressed in the body. Through characterization of promoters bound by EBF3 in neuronal cells, we saw enrichment for binding to NDD genes (p = 7.43 × 10 −6 , OR = 1.87) involved in gene regulation. Individuals with coding DNVs have greater phenotypic severity (hypotonia, ataxia, and delayed development syndrome [HADDS]) in comparison to individuals with noncoding DNVs that have autism and hypotonia. Conclusions In this study, we identify DNVs in the hs737 enhancer in individuals with autism. Through multiple approaches, we find hs737 targets the gene EBF3 that is genome-wide significant in NDDs. By assessment of noncoding variation and the genes they affect, we are beginning to understand their impact on gene regulatory networks in NDDs.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Functional and comparative genomics reveals conserved noncoding sequences in the nitrogen–fixing clade

Nitrogen is one of the most inaccessible plant nutrients, but certain species have overcome this limitation by establishing symbiotic interactions with nitrogen-fixing bacteria in the root nodule. This root–nodule symbiosis (RNS) is restricted to species within a single clade of angiosperms, suggesting a critical, but undetermined, evolutionary event at the base of this clade. To identify putative regulatory sequences implicated in the evolution of RNS, we evaluated the genomes of 25 species capable of nodulation and identified 3091 conserved noncoding sequences (CNS) in the nitrogen-fixing clade (NFC). We show that the chromatin accessibility of 452 CNS correlates significantly with the regulation of genes responding to lipochitooligosaccharides in Medicago truncatula. These included 38 CNS in proximity to 19 known genes involved in RNS. Five such regions are upstream of MtCRE1, Cytokinin Response Element 1, required to activate a suite of downstream transcription factors necessary for nodulation in M. truncatula. Genetic complementation of an Mtcre1 mutant showed a significant decrease of nodulation in the absence of the five CNS, when they are driving the expression of a functional copy of MtCRE1. CNS identified in the NFC may harbor elements required for the regulation of genes controlling RNS in M. truncatula.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2021

Synaptonemal complex formation produces a particular arrangement of the lateral element-associated DNA

Highlights: • The NAMA-Ur method can be used to analyze the DNA associated to the synaptonemal complex. • The DNA associated to the synaptonemal complex display bubble-like organization. • Formation of the synaptonemal complex is enough to produce the bubble-like organization of the DNA. • Synaptonemal complex without lateral elements produce similar organization of its associated DNA. During meiosis, homologous chromosomes exchange genetic material. This exchange or meiotic recombination is mediated by a proteinaceous scaffold known as the Synaptonemal complex (SC). Any defects in its formation produce failures in meiotic recombination, chromosome segregation and meiosis completion. It has been proposed that DNA repair events that will be resolved by crossover between homologous chromosomes are predetermined by the SC. Hence, structural analysis of the organization of the DNA in the SC could shed light on the process of crossover interference. In this work, we employed an ultrastructural DNA staining technique on mouse testis and followed nuclei of pachytene cells. We observed structures organized similarly to the SCs stained with conventional techniques. These structures, presumably the DNA in the SCs, are delineating the edges of both lateral elements and no staining was observed between them. DNA in the LEs resembles two parallel tracks. However, a bubble-like staining pattern in certain regions of the SC was observed. Furthermore, this staining pattern is found in SCs formed between non-homologous chromosomes, in SCs formed between sister chromatids and in SCs without lateral elements, suggesting that this particular organization of the DNA is determined by the synapsis of the chromosomes despite their lack of homology or the presence of partially formed SCs.

60 APPLIED LIFE SCIENCES↗

DOE OSTI2020

The uncharacterized gene EVE contributes to vessel element dimensions in Populus

The radiation of angiosperms led to the emergence of the vast majority of today’s plant species and all our major food crops. Their extraordinary diversification occurred in conjunction with the evolution of a more efficient vascular system for the transport of water, composed of vessel elements. The physical dimensions of these water-conducting specialized cells have played a critical role in angiosperm evolution; they determine resistance to water flow, influence photosynthesis rate, and contribute to plant stature. However, the genetic factors that determine their dimensions are unclear. Here we show that a previously uncharacterized gene, ENLARGED VESSEL ELEMENT ( EVE ) , contributes to the dimensions of vessel elements in Populus , impacting hydraulic conductivity. Our data suggest that EVE is localized in the plasma membrane and is involved in potassium uptake of differentiating xylem cells during vessel development. In plants, EVE first emerged in streptophyte algae, but expanded dramatically among vessel-containing angiosperms. The phylogeny, structure and composition of EVE indicates that it may have been involved in an ancient horizontal gene-transfer event.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Multiple origins, one evolutionary trajectory: gradual evolution characterizes distinct lineages of allotetraploid Brachypodium

The “genomic shock” hypothesis posits that unusual challenges to genome integrity such as whole genome duplication may induce chaotic genome restructuring. Decades of research on polyploid genomes have revealed that this is often, but not always the case. While some polyploids show major chromosomal rearrangements and derepression of transposable elements in the immediate aftermath of whole genome duplication, others do not. Nonetheless, all polyploids show gradual diploidization over evolutionary time. To evaluate these hypotheses, we produced a chromosome-scale reference genome for the natural allotetraploid grass Brachypodium hybridum, accession “Bhyb26.” We compared 2 independently derived accessions of B. hybridum and their deeply diverged diploid progenitor species Brachypodium stacei and Brachypodium distachyon. The 2 B. hybridum lineages provide a natural timecourse in genome evolution because one formed 1.4 million years ago, and the other formed 140 thousand years ago. The genome of the older lineage reveals signs of gradual post-whole genome duplication genome evolution including minor gene loss and genome rearrangement that are missing from the younger lineage. In neither B. hybridum lineage do we find signs of homeologous recombination or pronounced transposable element activation, though we find evidence supporting steady post-whole genome duplication transposable element activity in the older lineage. Gene loss in the older lineage was slightly biased toward 1 subgenome, but genome dominance was not observed at the transcriptomic level. We propose that relaxed selection, rather than an abrupt genomic shock, drives evolutionary novelty in B. hybridum, and that the progenitor species’ similarity in transposable element load may account for the subtlety of the observed genome dominance.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Modeling for the phased injector upgrade for 12 GeV CEBAF

The upcoming Jefferson Lab K-Long experiment at Hall D will require unique beam conditions with a much lower bunch repetition rate and atypically high bunch charge. To optimize the Continuous Electron Beam Accelerator Facility (CEBAF) injector for this experiment, we performed Multi-Objective Genetic Optimization (MGO) using General Particle Tracer (GPT) to determine the magnetic elements and RF settings necessary for the K-long bunch charge (0.64 pC) at 200 kV. We also investigated the transmission and beam characteristics of low to high charge per bunch electron beams through the injector for simultaneous operations of all four CEBAF Halls and characterized the transmission as a function of the photocathode laser spot size and pulse length. Our findings provide valuable insights into optimizing the CEBAF injector for the Jefferson Lab K-Long experiment, as well as for other experiments with similar beam conditions

Kazimi, R.↗

NASA NTRS1974

Radial and directional solidification of metallic systems in space

Investigation of the solidification behavior of spherical specimens of Ni-12 wt % Sn and Ni-1 wt % Ag that froze radially from the surface toward the center and cylindrical specimens of Al-33 wt % Cu eutectic that froze directionally under appropriately selected conditions of thermal gradient at the solid-liquid interface and growth rate. Possible effects of vacuum and low gravity conditions, under which the spherical specimens were processed, on observed nucleation and growth phenomena are discussed. A genetic explanation is given of observed microstructures, and the distributions of alloying elements is discussed. In directionally solidified eutectic specimens a comparison is made between statistically evaluated growth defects in Skylab and in ground specimens.

Katamis, T. Z.↗

NASA NTRS1992

Origin of giant Martian polygons

Extensive areas of the Martian northern plains in Utopia and Acidalia planitiae are characterized by 'polygonal terrane'. Polygonal terrane consists of material cut by complex troughs defining a pattern resembling mudcracks, columnar joints, or frost-wedge polygons on earth. However, the Martian polygons are orders of magnitude larger than these potential earth analogues, leading to severe mechanical difficulties for genetic models based on simple analogy arguments. Plate-bending and finite element models indicate that shrinkage of desiccating sediment or cooling volcanics accompanied by differential compaction over buried topography can account for the stresses responsible for polygon troughs as well as the large size of the polygons. Although trough widths and depths relate primarily to shrinkage, the large scale of the polygonl pattern relates to the spacing between topographic elevations on the surface buried beneath polygonal terrane material. Geological relationships favor a sedimentary origin for polygonal terrane material, but our model is not dependent on the specific genesis. Our analysis also suggests that the polygons must have formed at a geologically rapid rate.

Mcgill, George E.↗

NASA NTRS1996

Excess nutrients in hydroponic solutions alter nutrient content of rice, wheat, and potato

Environment has significant effects on the nutrient content of field-grown crop plants. Little is known, however, about compositional changes caused by controlled environments in which plants receive only artificial radiation and soilless, hydroponic culture. This knowledge is essential for developing a safe, nutritious diet in a Controlled Ecological Life-Support System (CELSS). Three crops that are candidates for inclusion in a CELSS (rice, wheat, and white potato) were grown both in the field and in controlled environments where the hydroponic nutrient solution, photosynthetic photon flux (PPF), and CO2 level were manipulated to achieve rapid growth rates. Plants were harvested at maturity, separated into discrete parts, and dried prior to analysis. Plant materials were analyzed for proximate composition (protein, fat, ash, and carbohydrate), total nitrogen (N), nitrate, minerals, and amino-acid composition. The effect of environment on nutrient content varied by crop and plant part. Total N and nonprotein N (NPN) contents of plant biomass generally increased under controlled-environment conditions compared to field conditions, especially for leafy plant parts and roots. Nitrate levels were increased in hydroponically-grown vegetative tissues, but nitrate was excluded from grains and tubers. Mineral content changes in plant tissue included increased phosphorus and decreased levels of certain micronutrient elements under controlled-environment conditions. These findings suggest that cultivar selection, genetic manipulation, and environmental control could be important to obtain highly nutritious biomass in a CELSS.

NASA Discipline Number 61-20↗

NASA NTRS2002

On the nature and evolution of the neural bases of human language

The traditional theory equating the brain bases of language with Broca's and Wernicke's neocortical areas is wrong. Neural circuits linking activity in anatomically segregated populations of neurons in subcortical structures and the neocortex throughout the human brain regulate complex behaviors such as walking, talking, and comprehending the meaning of sentences. When we hear or read a word, neural structures involved in the perception or real-world associations of the word are activated as well as posterior cortical regions adjacent to Wernicke's area. Many areas of the neocortex and subcortical structures support the cortical-striatal-cortical circuits that confer complex syntactic ability, speech production, and a large vocabulary. However, many of these structures also form part of the neural circuits regulating other aspects of behavior. For example, the basal ganglia, which regulate motor control, are also crucial elements in the circuits that confer human linguistic ability and abstract reasoning. The cerebellum, traditionally associated with motor control, is active in motor learning. The basal ganglia are also key elements in reward-based learning. Data from studies of Broca's aphasia, Parkinson's disease, hypoxia, focal brain damage, and a genetically transmitted brain anomaly (the putative "language gene," family KE), and from comparative studies of the brains and behavior of other species, demonstrate that the basal ganglia sequence the discrete elements that constitute a complete motor act, syntactic process, or thought process. Imaging studies of intact human subjects and electrophysiologic and tracer studies of the brains and behavior of other species confirm these findings. As Dobzansky put it, "Nothing in biology makes sense except in the light of evolution" (cited in Mayr, 1982). That applies with as much force to the human brain and the neural bases of language as it does to the human foot or jaw. The converse follows: the mark of evolution on the brains of human beings and other species provides insight into the evolution of the brain bases of human language. The neural substrate that regulated motor control in the common ancestor of apes and humans most likely was modified to enhance cognitive and linguistic ability. Speech communication played a central role in this process. However, the process that ultimately resulted in the human brain may have started when our earliest hominid ancestors began to walk.

Review, Tutorial↗

DOE OSTI2022

Novel cis-regulatory elements as synthetic promoters to drive recombinant protein expression from the Chlamydomonas reinhardtii nuclear genome

Eukaryotic green microalgae represent a sustainable, photosynthetic biotechnology platform for generating high-value products. The model green alga Chlamydomonas reinhardtii has already been used to generate high value bioproducts such as recombinant proteins and terpenoids. However, low, unstable, and variable nuclear transgene expression has limited the ease and speed of metabolic engineering and recombinant protein expression in this system. Here, novel genetic devices for transgene expression in C. reinhardtii have been developed by identifying cis-regulatory DNA elements capable of driving high transgene expression in C. reinhardtii promoters using de novo motif discovery informatics approaches. Thirteen putative motifs were synthesized as concatemers, linked to a common minimal basal promoter, and assayed for their activity to drive expression of a yellow fluorescent protein reporter gene. Following transformation of the vectors into C. reinhardtii by electroporation, in vivo measurements of yellow fluorescent protein expression by flow cytometry revealed that five of the DNA motifs analyzed displayed significantly higher reporter expression compared to the basal promoter control. Two of the concatemerized motifs, despite being much smaller minimal cis-regulatory elements, drove reporter expression at levels approaching that of the conventionally-used AR1 promoter. This analysis provides insight into C. reinhardtii promoter structure and gene regulation, and provides a new toolbox of cis-regulatory elements that can be used to drive transgene expression at a variety of expression levels.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Speciation Underpinned by Unexpected Molecular Diversity in the Mycorrhizal Fungal Genus Pisolithus

The mutualistic ectomycorrhizal (ECM) fungal genus Pisolithus comprises 19 species defined to date which colonize the roots of >50 hosts worldwide suggesting that substantial genomic and functional evolution occurred during speciation. To better understand this intra-genus variation, we undertook a comparative multi-omic study of nine Pisolithus species sampled from North America, South America, Asia, and Australasia. We found that there was a small core set of genes common to all species (13%), and that these genes were more likely to be significantly regulated during symbiosis with a host than accessory or species-specific genes. Thus, the genetic “toolbox” foundational to the symbiotic lifestyle in this genus is small. Transposable elements were located significantly closer to gene classes including effector-like small secreted proteins (SSPs). Poorly conserved SSPs were more likely to be induced by symbiosis, suggesting that they may be a class of protein that tune host specificity. The Pisolithus gene repertoire is characterized by divergent CAZyme profiles when compared with other fungi, both symbiotic and saprotrophic. This was driven by differences in enzymes associated with symbiotic sugar processing, although metabolomic analysis suggest that neither copy number nor expression of these genes is sufficient to predict sugar capture from a host plant or its metabolism in fungal hyphae. Our results demonstrate that intra-genus genomic and functional diversity within ECM fungi is greater than previously thought, underlining the importance of continued comparative studies within the fungal tree of life to refine our focus on pathways and evolutionary processes foundational to this symbiotic lifestyle.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

VISTA Enhancer browser: an updated database of tissue-specific developmental enhancers

Regulatory elements (enhancers) are major drivers of gene expression in mammals and harbor many genetic variants associated with human diseases. Here, we present an updated VISTA Enhancer Browser (https://enhancer.lbl.gov), a database of transgenic enhancer assays conducted in developing mouse embryos in vivo. Since the original publication in 2007, the database grew nearly 20-fold from 250 to over 4500 experiments and currently harbors over 23 500 images. The updated database provides structured information on experiments conducted at different stages of embryonic development, including enhancer activities of human pathogenic and synthetic variants and sequences derived from a variety of species. In addition to manually curated results of thousands of individual experiments, the new database also features hundreds of manually curated comparisons between alleles. The VISTA Enhancer Browser provides a crucial resource for study of human genetic variation, gene regulation and developmental biology.

59 BASIC BIOLOGICAL SCIENCES↗