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DOE OSTI2022

Biomineralization: Integrating mechanism and evolutionary history

Calcium carbonate (CaCO 3 ) biomineralizing organisms have played major roles in the history of life and the global carbon cycle during the past 541 Ma. Both marine diversification and mass extinctions reflect physiological responses to environmental changes through time. An integrated understanding of carbonate biomineralization is necessary to illuminate this evolutionary record and to understand how modern organisms will respond to 21st century global change. Biomineralization evolved independently but convergently across phyla, suggesting a unity of mechanism that transcends biological differences. In this review, we combine CaCO 3 skeleton formation mechanisms with constraints from evolutionary history, omics, and a meta-analysis of isotopic data to develop a plausible model for CaCO 3 biomineralization applicable to all phyla. The model provides a framework for understanding the environmental sensitivity of marine calcifiers, past mass extinctions, and resilience in 21st century acidifying oceans. Thus, it frames questions about the past, present, and future of CaCO 3 biomineralizing organisms.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2023

Evolutionary consequences of nascent multicellular life cycles

A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing ‘snowflake’ yeast (Δace2/∆ace2) and aggregative ‘floc’ yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift—a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.

Life Sciences & Biomedicine - Other Topics↗
DOE OSTI2021

Potentiating antibiotic efficacy via perturbation of non-essential gene expression

Proliferation of multidrug-resistant (MDR) bacteria poses a threat to human health, requiring new strategies. Here we propose using fitness neutral gene expression perturbations to potentiate antibiotics. We systematically explored 270 gene knockout-antibiotic combinations in Escherichia coli, identifying 90 synergistic interactions. Identified gene targets were subsequently tested for antibiotic synergy on the transcriptomic level via multiplexed CRISPR-dCas9 and showed successful sensitization of E. coli without a separate fitness cost. These fitness neutral gene perturbations worked as co-therapies in reducing a Salmonella enterica intracellular infection in HeLa. Finally, these results informed the design of four antisense peptide nucleic acid (PNA) co-therapies, csgD, fnr, recA and acrA, against four MDR, clinically isolated bacteria. PNA combined with sub-minimal inhibitory concentrations of trimethoprim against two isolates of Klebsiella pneumoniae and E. coli showed three cases of re-sensitization with minimal fitness impacts. Our results highlight a promising approach for extending the utility of current antibiotics.

60 APPLIED LIFE SCIENCES↗
DOE OSTI2024

Hot springs viruses at Yellowstone National Park have ancient origins and are adapted to thermophilic hosts

Geothermal springs house unicellular red algae in the class Cyanidiophyceae that dominate the microbial biomass at these sites. Little is known about host-virus interactions in these environments. We analyzed the virus community associated with red algal mats in three neighboring habitats (creek, endolithic, soil) at Lemonade Creek, Yellowstone National Park (YNP), USA. We find that despite proximity, each habitat houses a unique collection of viruses, with the giant viruses, Megaviricetes, dominant in all three. The early branching phylogenetic position of genes encoded on metagenome assembled virus genomes (vMAGs) suggests that the YNP lineages are of ancient origin and not due to multiple invasions from mesophilic habitats. The existence of genomic footprints of adaptation to thermophily in the vMAGs is consistent with this idea. The Cyanidiophyceae at geothermal sites originated ca. 1.5 Bya and are therefore relevant to understanding biotic interactions on the early Earth.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Real-time tracking of protein unfolding with time-resolved x-ray solution scattering

The correct folding of proteins is of paramount importance for their function, and protein misfolding is believed to be the primary cause of a wide range of diseases. Protein folding has been investigated with time-averaged methods and time-resolved spectroscopy, but observing the structural dynamics of the unfolding process in real-time is challenging. Here, we demonstrate an approach to directly reveal the structural changes in the unfolding reaction. We use nano- to millisecond time-resolved x-ray solution scattering to probe the unfolding of apomyoglobin. The unfolding reaction was triggered using a temperature jump, which was induced by a nanosecond laser pulse. We demonstrate a new strategy to interpret time-resolved x-ray solution scattering data, which evaluates ensembles of structures obtained from molecular dynamics simulations. We find that apomyoglobin passes three states when unfolding, which we characterize as native, molten globule, and unfolded. The molten globule dominates the population under the conditions investigated herein, whereas native and unfolded structures primarily contribute before the laser jump and 30 μs after it, respectively. The molten globule retains much of the native structure but shows a dynamic pattern of inter-residue contacts. Our study demonstrates a new strategy to directly observe structural changes over the cause of the unfolding reaction, providing time- and spatially resolved atomic details of the folding mechanism of globular proteins.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Three-dimensional modeling of hyphal fusion, branching, and nutrient transport in filamentous fungi

Fungi exhibit behaviors distinct from other microbes. Filamentous fungi grow by extending complex networks of branched filaments collectively referred to as the mycelium. These networks can expand over large distances and traverse low-nutrient areas by translocating nutrients through the filament network. This spatial characteristic makes filamentous fungi crucial for soil ecosystems, supporting stable microbial communities and promoting plant growth. However, simulating these behaviors is complex. The elongated nature of fungal compartments results in different mechanical interactions compared to the commonly modeled spherical bacteria. These detailed hyphal mechanics require specialized consideration and are often excluded from conventional fungal simulation packages. Additionally, the extensive fungal networks in nature demand computationally intensive simulations, necessitating high-performance algorithms. Therefore, realistic fungi simulations require specialized software. Here, we introduce a fungal modeling expansion to the high-performance biological modelling and interface exchange (bmx) software suite. bmx leverages adaptive mesh refinement in AMReX for chemical diffusion and incorporates a full mechanical model for bacterial cells, accelerated by GPUs. By extending bmx to model filamentous particles, we demonstrate the formation of complex filament networks through interactions like hyphal branching and fusion (anastomosis). We show that the networks produced match real-world fungal structures through various metrics. This work supports computational studies of fungal growth dynamics and can be adapted to investigate the growth of other filamentous structures in biology or materials science. The expanded-BMX package is open-sourced and is available online.

Cell mechanics↗
DOE OSTI2021

Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution

When gene regulatory networks diverge between species, their dysfunctional expression in inter-species hybrid individuals can create genetic incompatibilities that generate the developmental defects responsible for intrinsic post-zygotic reproductive isolation. Both cis- and trans-acting regulatory divergence can be hastened by directional selection through adaptation, sexual selection, and inter-sexual conflict, in addition to cryptic evolution under stabilizing selection. Dysfunctional sex-biased gene expression, in particular, may provide an important source of sexually-dimorphic genetic incompatibilities. Here, we characterize and compare male and female/hermaphrodite transcriptome profiles for sibling nematode species Caenorhabditis briggsae and C. nigoni, along with allele-specific expression in their F 1 hybrids, to deconvolve features of expression divergence and regulatory dysfunction. Despite evidence of widespread stabilizing selection on gene expression, misexpression of sex-biased genes pervades F 1 hybrids of both sexes. This finding implicates greater fragility of male genetic networks to produce dysfunctional organismal phenotypes. Spermatogenesis genes are especially prone to high divergence in both expression and coding sequences, consistent with a “faster male” model for Haldane’s rule and elevated sterility of hybrid males. Moreover, underdominant expression pervades male-biased genes compared to female-biased and sex-neutral genes and an excess of cis-trans compensatory regulatory divergence for X-linked genes underscores a “large-X effect” for hybrid male expression dysfunction. Extensive regulatory divergence in sex determination pathway genes likely contributes to demasculinization of XX hybrids. The evolution of genetic incompatibilities due to regulatory versus coding sequence divergence, however, are expected to arise in an uncorrelated fashion. This study identifies important differences between the sexes in how regulatory networks diverge to contribute to sex-biases in how genetic incompatibilities manifest during the speciation process.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2025

Unique Structural Features Relate to Evolutionary Adaptation of Cytochrome P450 in the Abyssal Zone

Cytochromes P450 (CYPs) form one of the largest enzyme superfamilies, with similar structural folds yet biological functions varying from synthesis of physiologically essential compounds to metabolism of myriad xenobiotics. Sterol 14α-demethylases (CYP51s) represent a very special P450 family, regarded as a possible evolutionary progenitor for all currently existing P450s. In metazoans CYP51 is critical for the biosynthesis of sterols including cholesterol. Here we determined the crystal structures of ligand-free CYP51s from the abyssal fish Coryphaenoides armatus and human-. Comparative sequence–structure–function analysis revealed specific structural elements that imply elevated conformational flexibility, uncovering a molecular basis for faster catalytic rates, lower substrate selectivity, and intrinsic resistance to inhibition. In addition, the C. armatus structure displayed a large-scale repositioning of structural segments that, in vivo, are immersed in the endoplasmic reticulum membrane and border the substrate entrance (the FG arm, >20 Å, and the β4 hairpin, >15 Å). The structural distinction of C. armatus CYP51, which is the first structurally characterized deep sea P450, suggests stronger involvement of the membrane environment in regulation of the enzyme function. We interpret this as a co-adaptation of the membrane protein structure with membrane lipid composition during evolutionary incursion to life in the deep sea.

Biochemistry & Molecular Biology↗
DOE OSTI2020

The state of algal genome quality and diversity

The genomic era of biology has created unprecedented opportunity to study how life works, including understanding evolutionary principles, bioprospecting for novel antibiotics, and genetic manipulation of bioeconomically-relevant species. While genome sequencing and genomic analysis was previously restricted to large-scale projects and consortia, sequencing has become democratized. However, as genomics has become commonplace, the cataloging of sequenced organisms has become challenging, and standardized practices for sequencing, assembly, and annotation have not been adopted. This is equally true in research fields such as algal biology, despite the growing importance of algae in a bio-based economy. Here, in this study, we provide a comprehensive review of the state of eukaryotic algal genomics, explore the quality of algal genome assemblies, and identify the biases and gaps in the current species distribution to inform the development of future genome projects. Overall, we find a trend of declining quality of genomic resources, including a reduction in assembly quality, gene annotation quality, and genome completeness. Potential solutions to improve genome quality include widespread utilization of long read and scaffolding technologies, implementation of standards for assembly quality, evidence-based gene annotation and requisite publication, and support of continued development of gene prediction and genome assessment software.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Museomics Dissects the Genetic Basis for Adaptive Seasonal Coloration in the Least Weasel

Abstract Dissecting the link between genetic variation and adaptive phenotypes provides outstanding opportunities to understand fundamental evolutionary processes. Here, we use a museomics approach to investigate the genetic basis and evolution of winter coat coloration morphs in least weasels (Mustela nivalis), a repeated adaptation for camouflage in mammals with seasonal pelage color moults across regions with varying winter snow. Whole-genome sequence data were obtained from biological collections and mapped onto a newly assembled reference genome for the species. Sampling represented two replicate transition zones between nivalis and vulgaris coloration morphs in Europe, which typically develop white or brown winter coats, respectively. Population analyses showed that the morph distribution across transition zones is not a by-product of historical structure. Association scans linked a 200-kb genomic region to coloration morph, which was validated by genotyping museum specimens from intermorph experimental crosses. Genotyping the wild populations narrowed down the association to pigmentation gene MC1R and pinpointed a candidate amino acid change cosegregating with coloration morph. This polymorphism replaces an ancestral leucine residue by lysine at the start of the first extracellular loop of the protein in the vulgaris morph. A selective sweep signature overlapped the association region in vulgaris, suggesting that past adaptation favored winter-brown morphs and can anchor future adaptive responses to decreasing winter snow. Using biological collections as valuable resources to study natural adaptations, our study showed a new evolutionary route generating winter color variation in mammals and that seasonal camouflage can be modulated by changes at single key genes.

Miranda, Inês↗
DOE OSTI2022

Mass spectrometry-based technologies for probing the 3D world of plant proteins

Abstract Over the past two decades, mass spectrometric (MS)-based proteomics technologies have facilitated the study of signaling pathways throughout biology. Nowhere is this needed more than in plants, where an evolutionary history of genome duplications has resulted in large gene families involved in posttranslational modifications and regulatory pathways. For example, at least 5% of the Arabidopsis thaliana genome (ca. 1,200 genes) encodes protein kinases and protein phosphatases that regulate nearly all aspects of plant growth and development. MS-based technologies that quantify covalent changes in the side-chain of amino acids are critically important, but they only address one piece of the puzzle. A more crucially important mechanistic question is how noncovalent interactions—which are more difficult to study—dynamically regulate the proteome’s 3D structure. The advent of improvements in protein 3D technologies such as cryo-electron microscopy, nuclear magnetic resonance, and X-ray crystallography has allowed considerable progress to be made at this level, but these methods are typically limited to analyzing proteins, which can be expressed and purified in milligram quantities. Newly emerging MS-based technologies have recently been developed for studying the 3D structure of proteins. Importantly, these methods do not require protein samples to be purified and require smaller amounts of sample, opening the wider proteome for structural analysis in complex mixtures, crude lysates, and even in intact cells. These MS-based methods include covalent labeling, crosslinking, thermal proteome profiling, and limited proteolysis, all of which can be leveraged by established MS workflows, as well as newly emerging methods capable of analyzing intact macromolecules and the complexes they form. In this review, we discuss these recent innovations in MS-based “structural” proteomics to provide readers with an understanding of the opportunities they offer and the remaining challenges for understanding the molecular underpinnings of plant structure and function.

Plant Sciences↗
DOE OSTI2020

Training Spiking Neural Networks Using Combined Learning Approaches

Spiking neural networks (SNNs), the class of neural networks used in neuromorphic computing, are difficult to train using traditional back-propagation techniques. Spike timingdependent plasticity (STDP) is a biologically inspired learning mechanism that can be used to train SNNs. Evolutionary algorithms have also been demonstrated as a method for training SNNs. In this work, we explore the relationship between these two training methodologies. We evaluate STDP and evolutionary optimization as standalone methods for training networks, and also evaluate a combined approach where STDP weight updates are applied within an evolutionary algorithm. We also apply Bayesian hyperparameter optimization as a meta learner for each of the algorithms. We find that STDP by itself is not an ideal learning rule for randomly connected networks, while the inclusion of STDP within an evolutionary algorithm leads to similar performance, with a few interesting differences. This study suggests future work in understanding the relationship between network topology and learning rules.

Elbrecht, Daniel↗
DOE OSTI2020

Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases

Magnetotactic bacteria (MTB) are prokaryotes that possess genes for the synthesis of membrane-bounded crystals of magnetite or greigite, called magnetosomes. Despite over half a century of studying MTB, only about 60 genomes have been sequenced. Most belong to Proteobacteria, with a minority affiliated with the Nitrospirae, Omnitrophica, Planctomycetes, and Latescibacteria. Due to the scanty information available regarding MTB phylogenetic diversity, little is known about their ecology, evolution and about the magnetosome biomineralization process. This study presents a large-scale search of magnetosome biomineralization genes and reveals 38 new MTB genomes. Several of these genomes were detected in the phyla Elusimicrobia, Candidatus Hydrogenedentes, and Nitrospinae, where magnetotactic representatives have not previously been reported. Analysis of the obtained putative magnetosome biomineralization genes revealed a monophyletic origin capable of putative greigite magnetosome synthesis. The ecological distributions of the reconstructed MTB genomes were also analyzed and several patterns were identified. These data suggest that open databases are an excellent source for obtaining new information of interest.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2020

Inference of Chromosome-Length Haplotypes Using Genomic Data of Three or a Few More Single Gametes

Compared with genomic data of individual markers, haplotype data provide higher resolution for DNA variants, advancing our knowledge in genetics and evolution. Although many computational and experimental phasing methods have been developed for analyzing diploid genomes, it remains challenging to reconstruct chromosome-scale haplotypes at low cost, which constrains the utility of this valuable genetic resource. Gamete cells, the natural packaging of haploid complements, are ideal materials for phasing entire chromosomes because the majority of the haplotypic allele combinations has been preserved. Therefore, compared with the current diploid-based phasing methods, using haploid genomic data of single gametes may substantially reduce the complexity in inferring the donor’s chromosomal haplotypes. In this study, we developed the first easy-to-use R package, Hapi, for inferring chromosome-length haplotypes of individual diploid genomes with only a few gametes. Hapi outperformed other phasing methods when analyzing both simulated and real single gamete cell sequencing data sets. The results also suggested that chromosome-scale haplotypes may be inferred by using as few as three gametes, which has pushed the boundary to its possible limit. The single gamete cell sequencing technology allied with the cost-effective Hapi method will make large-scale haplotype-based genetic studies feasible and affordable, promoting the use of haplotype data in a wide range of research.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2023

Opportunities to advance the synthesis of ecology and evolution

Despite decades of research on the interactions between ecology and evolution, opportunities still remain to further integrate the two disciplines, especially when considering multispecies systems. Here, we discuss two such opportunities. First, the traditional emphasis on the distinction between evolutionary and ecological processes should be further relaxed as it is particularly unhelpful in the study of microbial communities, where the very notion of species is hard to define. Second, key processes of evolutionary theory such as adaptation should be exported to hierarchical levels higher than populations to make sense of biodiversity dynamics. Together, we argue that broadening our perspective of eco-evolutionary dynamics to be more inclusive of all biodiversity, both phylogenetically and hierarchically, will open up fertile new research directions and help us to address one of the major scientific challenges of our time, that is, to understand and predict changes in biodiversity in the face of rapid environmental change.

54 ENVIRONMENTAL SCIENCES↗
DOE OSTI2026

Convergent evolution of aerobic fermentation through divergent mechanisms acting on the same key glycolytic genes

Expression profiling by high throughput sequencing The model yeast Saccharomyces cerevisiae has evolved aerobic fermentation in part through a whole genome duplication and subsequent retention of glycolytic genes. To identify independent yeast lineages with a high glycolytic rate phenotype we developed an assay measuring extracellular acidification rates (ECAR) to evaluate the glycolytic rates across diverse yeast species. This assay identified a novel group of yeasts in the genus Saturnispora with rapid glycolytic rates. Through comparative approaches, we found that several glycolytic genes encoding hexokinases and enzymes in lower glycolysis had higher expression and modifications in promoter sequences in rapid ECAR species. Intriguingly, many of the upregulated genes are the same genes that are duplicated in S. cerevisiae. When the transcription factor required for their activation was deleted, the mutants had a slow glycolytic rate and more respiratory phenotype. This work shows how the aerobic fermentation phenotype has convergently evolved in Saturnispora through transcriptional rewiring. This divergent mechanism nevertheless impacts the same glycolytic genes, which suggests that there are evolutionary constraints on how aerobic fermentation can arise.

Horianopoulos, Linda C. [Department of Food Scienc↗
DOE OSTI2025

A compendium of human gene functions derived from evolutionary modelling

A comprehensive, computable representation of the functional repertoire of all macromolecules encoded within the human genome is a foundational resource for biology and biomedical research. The Gene Ontology Consortium has been working towards this goal by generating a structured body of information about gene functions, which now includes experimental findings reported in more than 175,000 publications for human genes and genes in experimentally tractable model organisms 1,2 . Here, we describe the results of a large, international effort to integrate all of these findings to create a representation of human gene functions that is as complete and accurate as possible. Specifically, we apply an expert-curated, explicit evolutionary modelling approach to all human protein-coding genes. This approach integrates available experimental information across families of related genes into models that reconstruct the gain and loss of functional characteristics over evolutionary time. The models and the resulting set of 68,667 integrated gene functions cover approximately 82% of human protein-coding genes. The functional repertoire reveals a marked preponderance of molecular regulatory functions, and the models provide insights into the evolutionary origins of human gene functions. We show that our set of descriptions of functions can improve the widely used genomic technique of Gene Ontology enrichment analysis. The experimental evidence for each functional characteristic is recorded, thereby enabling the scientific community to help review and improve the resource, which we have made publicly available.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Phytohormones in a universe of regulatory metabolites: lessons from jasmonate

Small-molecule phytohormones exert control over plant growth, development, and stress responses by coordinating the patterns of gene expression within and between cells. Increasing evidence indicates that currently recognized plant hormones are part of a larger group of regulatory metabolites that have acquired signaling properties during the evolution of land plants. This rich assortment of chemical signals reflects the tremendous diversity of plant secondary metabolism, which offers evolutionary solutions to the daunting challenges of sessility and other unique aspects of plant biology. A major gap in our current understanding of plant regulatory metabolites is the lack of insight into the direct targets of these compounds. Here, we illustrate the blurred distinction between classical phytohormones and other bioactive metabolites by highlighting the major scientific advances that transformed the view of jasmonate from an interesting floral scent to a potent transcriptional regulator. Lessons from jasmonate research generally apply to other phytohormones and thus may help provide a broad understanding of regulatory metabolite–protein interactions. In providing a framework that links small-molecule diversity to transcriptional plasticity, we hope to stimulate future research to explore the evolution, functions, and mechanisms of perception of a broad range of plant regulatory metabolites.

59 BASIC BIOLOGICAL SCIENCES↗