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All sourcesNASA NTRSDOE OSTI
NASA NTRS1998

The origin and evolution of oxygenic photosynthesis

The evolutionary developments that led to the ability of photosynthetic organisms to oxidize water to molecular oxygen are discussed. Two major changes from a more primitive non-oxygen-evolving reaction center are required: a charge-accumulating system and a reaction center pigment with a greater oxidizing potential. Intermediate stages are proposed in which hydrogen peroxide was oxidized by the reaction center, and an intermediate pigment, similar to chlorophyll d, was present.

Review, Tutorial↗
NASA NTRS2013

Phylogenetic Conservatism in Plant Phenology

Phenological events defined points in the life cycle of a plant or animal have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. Here, we evaluated evidence for phylogenetic conservatism the tendency for closely related species to share similar ecological and biological attributes in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing 4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the set of included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. We show that more closely related species tend to flower and leaf at similar times. By contrasting mean flowering times within and across sites, however, we illustrate that it is not the time of year that is conserved, but rather the phenological responses to a common set of abiotic cues. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses.Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conserved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species' shared evolutionary histories.

phylogenetic conservatism↗
DOE OSTI2023

Mycoparasites, Gut Dwellers, and Saprotrophs: Phylogenomic Reconstructions and Comparative Analyses of Kickxellomycotina Fungi

Improved sequencing technologies have profoundly altered global views of fungal diversity and evolution. High-throughput sequencing methods are critical for studying fungi due to the cryptic, symbiotic nature of many species, particularly those that are difficult to culture. However, the low coverage genome sequencing (LCGS) approach to phylogenomic inference has not been widely applied to fungi. Here we analyzed 171 Kickxellomycotina fungi using LCGS methods to obtain hundreds of marker genes for robust phylogenomic reconstruction. Additionally, we mined our LCGS data for a set of nine rDNA and protein coding genes to enable analyses across species for which no LCGS data were obtained. The main goals of this study were to: 1) evaluate the quality and utility of LCGS data for both phylogenetic reconstruction and functional annotation, 2) test relationships among clades of Kickxellomycotina, and 3) perform comparative functional analyses between clades to gain insight into putative trophic modes. In opposition to previous studies, our nine-gene analyses support two clades of arthropod gut dwelling species and suggest a possible single evolutionary event leading to this symbiotic lifestyle. Furthermore, we resolve the mycoparasitic Dimargaritales as the earliest diverging clade in the subphylum and find four major clades of Coemansia species. Finally, functional analyses illustrate clear variation in predicted carbohydrate active enzymes and secondary metabolites (SM) based on ecology, that is biotroph versus saprotroph. Saprotrophic Kickxellales broadly lack many known pectinase families compared with saprotrophic Mucoromycota and are depauperate for SM but have similar numbers of predicted chitinases as mycoparasitic.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2022

A 2-million-year-old ecosystem in Greenland uncovered by environmental DNA

Late Pliocene and Early Pleistocene epochs 3.6 to 0.8 million years ago had climates resembling those forecasted under future warming. Palaeoclimatic records show strong polar amplification with mean annual temperatures of 11–19 °C above contemporary values. The biological communities inhabiting the Arctic during this time remain poorly known because fossils are rare. Here we report an ancient environmental DNA (eDNA) record describing the rich plant and animal assemblages of the Kap København Formation in North Greenland, dated to around two million years ago. The record shows an open boreal forest ecosystem with mixed vegetation of poplar, birch and thuja trees, as well as a variety of Arctic and boreal shrubs and herbs, many of which had not previously been detected at the site from macrofossil and pollen records. The DNA record confirms the presence of hare and mitochondrial DNA from animals including mastodons, reindeer, rodents and geese, all ancestral to their present-day and late Pleistocene relatives. The presence of marine species including horseshoe crab and green algae support a warmer climate than today. The reconstructed ecosystem has no modern analogue. The survival of such ancient eDNA probably relates to its binding to mineral surfaces. Our findings open new areas of genetic research, demonstrating that it is possible to track the ecology and evolution of biological communities from two million years ago using ancient eDNA.

58 GEOSCIENCES↗
DOE OSTI2022

Engineered human antibodies for the opsonization and killing of Staphylococcus aureus

Gram-positive organisms with their thick envelope cannot be lysed by complement alone. Nonetheless, antibody-binding on the surface can recruit complement and mark these invaders for uptake and killing by phagocytes, a process known as opsonophagocytosis. The crystallizable fragment of immunoglobulins (Fcγ) is key for complement recruitment. The cell surface of S. aureus is coated with Staphylococcal protein A (SpA). SpA captures the Fcγ domain of IgG and interferes with opsonization by anti-S. aureus antibodies. In principle, the Fcγ domain of therapeutic antibodies could be engineered to avoid the inhibitory activity of SpA. However, the SpA-binding site on Fcγ overlaps with that of the neonatal Fc receptor (FcRn), an interaction that is critical for prolonging the half-life of serum IgG. This evolutionary adaptation poses a challenge for the exploration of Fcγ mutants that can both weaken SpA–IgG interactions and retain stability. Here, we use both wild-type and transgenic human FcRn mice to identify antibodies with enhanced half-life and increased opsonophagocytic killing in models of S. aureus infection and demonstrate that antibody-based immunotherapy can be improved by modifying Fcγ. Our experiments also show that by competing for FcRn-binding, staphylococci effectively reduce the half-life of antibodies during infection. These observations may have profound impact in treating cancer, autoimmune, and asthma patients colonized or infected with S. aureus and undergoing monoclonal antibody treatment.

59 BASIC BIOLOGICAL SCIENCES↗
NASA NTRS1975

Theoretical and experimental prerequisites of exobiology

Exobiology and the origin of life: The Inseparable Connection The world we live in is constantly changing through a process of evolutionary development that is gradual, and which leads to emergence of ever newer, more complex, more diverse, and richly differentiated forms of reality. This process may not occur simultaneously and identically everywhere, but in different ways at different rates in various places in the universe and on various objects in the celestial world. Thus, evolution must not be diagramed as a single direct line, but rather as a cluster of various paths, whose separate branches may lead to very complex and complete forms of organization and movement of matter. Nothing is known about many of these forms, and in numerous instances, their existence is not even suspected. Any one form should not be considered prematurely as a special category of life, only because of its complexity or perfection. Life is far from a result of all the numerous branches in the development of matter; its specific qualities and ways of emerging and improving are inherent. Only a single example of life, terrestrial life, is known at present, from which judgments must proceed of other possible forms of biological organization. The Earth and the events which originated on it must, to a great extent, serve as a model for broader judgments of life in the universe.

A. I. Oparin↗
DOE OSTI2024

Global characterization of biosynthetic gene clusters in non-model eukaryotes using domain architectures

Abstract The majority of pharmaceuticals are derived from natural products, bioactive compounds naturally synthesized by organisms to provide evolutionary advantages. Although the rich evolutionary history of eukaryotic algal species implicates a high potential for natural product-based drug discovery, it remains largely untouched. This study investigates 2762 putative biosynthetic gene clusters (BGCs) from 212 eukaryotic algal genomes. To analyze a vast set of structurally diverse BGCs, we employed comparative analysis based on the vectorization of biosynthetic domains, referred to as biosynthetic domain architecture (BDA). By characterizing core biosynthetic machineries through BDA, we identified key BDAs of modular BGCs in diverse eukaryotes and introduced 16 candidate modular BGCs with similar BDAs to previously validated BGCs. This study provides a global characterization of eukaryotic algal BGCs, offering an alternative to laborious manual curation for BGC prioritization.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

ECNet is an evolutionary context-integrated deep learning framework for protein engineering

Abstract Machine learning has been increasingly used for protein engineering. However, because the general sequence contexts they capture are not specific to the protein being engineered, the accuracy of existing machine learning algorithms is rather limited. Here, we report ECNet (evolutionary context-integrated neural network), a deep-learning algorithm that exploits evolutionary contexts to predict functional fitness for protein engineering. This algorithm integrates local evolutionary context from homologous sequences that explicitly model residue-residue epistasis for the protein of interest with the global evolutionary context that encodes rich semantic and structural features from the enormous protein sequence universe. As such, it enables accurate mapping from sequence to function and provides generalization from low-order mutants to higher-order mutants. We show that ECNet predicts the sequence-function relationship more accurately as compared to existing machine learning algorithms by using ~50 deep mutational scanning and random mutagenesis datasets. Moreover, we used ECNet to guide the engineering of TEM-1 β-lactamase and identified variants with improved ampicillin resistance with high success rates.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Novel symmetry-preserving neural network model for phylogenetic inference

Abstract Motivation Scientists world-wide are putting together massive efforts to understand how the biodiversity that we see on Earth evolved from single-cell organisms at the origin of life and this diversification process is represented through the Tree of Life. Low sampling rates and high heterogeneity in the rate of evolution across sites and lineages produce a phenomenon denoted “long branch attraction” (LBA) in which long nonsister lineages are estimated to be sisters regardless of their true evolutionary relationship. LBA has been a pervasive problem in phylogenetic inference affecting different types of methodologies from distance-based to likelihood-based. Results Here, we present a novel neural network model that outperforms standard phylogenetic methods and other neural network implementations under LBA settings. Furthermore, unlike existing neural network models in phylogenetics, our model naturally accounts for the tree isomorphisms via permutation invariant functions which ultimately result in lower memory and allows the seamless extension to larger trees. Availability and implementation We implement our novel theory on an open-source publicly available GitHub repository: https://github.com/crsl4/nn-phylogenetics.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Genome organization and botanical diversity

Abstract The rich diversity of angiosperms, both the planet's dominant flora and the cornerstone of agriculture, is integrally intertwined with a distinctive evolutionary history. Here, we explore the interplay between angiosperm genome organization and botanical diversity, empowered by genomic approaches ranging from genetic linkage mapping to analysis of gene regulation. Commonality in the genetic hardware of plants has enabled robust comparative genomics that has provided a broad picture of angiosperm evolution and implicated both general processes and specific elements in contributing to botanical diversity. We argue that the hardware of plant genomes—both in content and in dynamics—has been shaped by selection for rather substantial differences in gene regulation between plants and animals such as maize and human, organisms of comparable genome size and gene number. Their distinctive genome content and dynamics may reflect in part the indeterminate development of plants that puts strikingly different demands on gene regulation than in animals. Repeated polyploidization of plant genomes and multiplication of individual genes together with extensive rearrangement and differential retention provide rich raw material for selection of morphological and/or physiological variations conferring fitness in specific niches, whether natural or artificial. These findings exemplify the burgeoning information available to employ in increasing knowledge of plant biology and in modifying selected plants to better meet human needs.

Biochemistry & Molecular Biology↗
DOE OSTI2020

P finder: genomic and metagenomic annotation of RNase P RNA gene (rnpB)

Abstract Background The rnpB gene encodes for an essential catalytic RNA (RNase P). Like other essential RNAs, RNase P’s sequence is highly variable. However, unlike other essential RNAs (i.e. tRNA, 16 S, 6 S,...) its structure is also variable with at least 5 distinct structure types observed in prokaryotes. This structural variability makes it labor intensive and challenging to create and maintain covariance models for the detection of RNase P RNA in genomic and metagenomic sequences. The lack of a facile and rapid annotation algorithm has led to the rnpB gene being the most grossly under annotated essential gene in completed prokaryotic genomes with only a 24% annotation rate. Here we describe the coupling of the largest RNase P RNA database with the local alignment scoring algorithm to create the most sensitive and rapid prokaryote rnpB gene identification and annotation algorithm to date. Results Of the 2772 completed microbial genomes downloaded from GenBank only 665 genomes had an annotated rnpB gene. We applied P Finder to these genomes and were able to identify 2733 or nearly 99% of the 2772 microbial genomes examined. From these results four new rnpB genes that encode the minimal T-type P RNase P RNAs were identified computationally for the first time. In addition, only the second C-type RNase P RNA was identified in Sphaerobacter thermophilus . Of special note, no RNase P RNAs were detected in several obligate endosymbionts of sap sucking insects suggesting a novel evolutionary adaptation. Conclusions The coupling of the largest RNase P RNA database and associated structure class identification with the P Finder algorithm is both sensitive and rapid, yielding high quality results to aid researchers annotating either genomic or metagenomic data. It is the only algorithm to date that can identify challenging RNAse P classes such as C-type and the minimal T-type RNase P RNAs. P Finder is written in C# and has a user-friendly GUI that can run on multiple 64-bit windows platforms (Windows Vista/7/8/10). P Finder is free available for download at https://github.com/JChristopherEllis/P-Finder as well as a small sample RNase P RNA file for testing.

59 BASIC BIOLOGICAL SCIENCES↗
NASA NTRS2002

Monolignol radical-radical coupling networks in western red cedar and Arabidopsis and their evolutionary implications

The discovery of a nine-member multigene dirigent family involved in control of monolignol radical-radical coupling in the ancient gymnosperm, western red cedar, suggested that a complex multidimensional network had evolved to regulate such processes in vascular plants. Accordingly, in this study, the corresponding promoter regions for each dirigent multigene member were obtained by genome-walking, with Arabidopsis being subsequently transformed to express each promoter fused to the beta-glucuronidase (GUS) reporter gene. It was found that each component gene of the proposed network is apparently differentially expressed in individual tissues, organs and cells at all stages of plant growth and development. The data so obtained thus further support the hypothesis that a sophisticated monolignol radical-radical coupling network exists in plants which has been highly conserved throughout vascular plant evolution.

NASA Discipline Plant Biology↗
DOE OSTI2021

Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm

Researchers worldwide are repeatedly warning us against future zoonotic diseases resulting from humankind’s insurgence into natural ecosystems. The same zoonotic pathogens that cause severe infections in a human host frequently fail to produce any disease outcome in their natural hosts. What precise features of the immune system enable natural reservoirs to carry these pathogens so efficiently? To understand these effects, we highlight the importance of tracing the evolutionary basis of pathogen tolerance in reservoir hosts, while drawing implications from their diverse physiological and life-history traits, and ecological contexts of host-pathogen interactions. Long-term co-evolution might allow reservoir hosts to modulate immunity and evolve tolerance to zoonotic pathogens, increasing their circulation and infectious period. Such processes can also create a genetically diverse pathogen pool by allowing more mutations and genetic exchanges between circulating strains, thereby harboring rare alive-on-arrival variants with extended infectivity to new hosts (i.e., spillover). Finally, we end by underscoring the indispensability of a large multidisciplinary empirical framework to explore the proposed link between evolved tolerance, pathogen prevalence, and spillover in the wild.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

Emergence of catalytic function in prebiotic information-coding polymers

Life as we know it relies on the interplay between catalytic activity and information processing carried out by biological polymers. Here we present a plausible pathway by which a pool of prebiotic information-coding oligomers could acquire an early catalytic function, namely sequence-specific cleavage activity. Starting with a system capable of non-enzymatic templated replication, we demonstrate that even non-catalyzed spontaneous cleavage would promote proliferation by generating short fragments that act as primers. Furthermore, we show that catalytic cleavage function can naturally emerge and proliferate in this system. Specifically, a cooperative catalytic network with four subpopulations of oligomers is selected by the evolution in competition with chains lacking catalytic activity. The cooperative system emerges through the functional differentiation of oligomers into catalysts and their substrates. The model is inspired by the structure of the hammerhead RNA enzyme as well as other DNA- and RNA-based enzymes with cleavage activity that readily emerge through natural or artificial selection. We identify the conditions necessary for the emergence of the cooperative catalytic network. In particular, we show that it requires the catalytic rate enhancement over the spontaneous cleavage rate to be at least 10 2 –10 3 , a factor consistent with the existing experiments. The evolutionary pressure leads to a further increase in catalytic efficiency. The presented mechanism provides an escape route from a relatively simple pairwise replication of oligomers toward a more complex behavior involving catalytic function. This provides a bridge between the information-first origin of life scenarios and the paradigm of autocatalytic sets and hypercycles, albeit based on cleavage rather than synthesis of reactants.

Tkachenko, Alexei V. (ORCID:000000031291243X)↗
NASA NTRS1993

The RNA World: Life Before DNA and Protein

All of the life that is known, all organisms that exist on Earth today or are known to have existed on Earth in the past, are of the same life form: a life form based on DNA and protein. It does not necessarily have to be that way. Why not have two competing life forms on this planet? Why not have biology as we know it and some other biology that occupies its own distinct niche? Yet that is not how evolution has played out. From microbes living on the surface of antarctic ice to tube worms lying near the deep-sea hydrothermal vents, all known organisms on this planet are of the same biology. Looking at the single known biology on Earth, it is clear that this biology could not have simply sprung forth from the primordial soup. The biological system that is the basis for all known. life is far too complicated to have arisen spontaneously. This brings us to the notion that something else something simpler, must have preceded life based on DNA and protein. One suggestion that has gained considerable acceptance over the past decade is that DNA and protein-based life was preceded by RNA-based life in a period referred to as the 'RNA world'. Even an RNA-based life form would have been fairly complicated - not as complicated as our own DNA- and protein-based life form - but far too complicated, according to prevailing scientific thinking, to have arisen spontaneously from the primordial soup. Thus, it has been argued that something else must have preceded RNA-based life, or even that there was a succession of life forms leading from the primordial soup to RNA-based life. The experimental evidence to support this conjecture is not strong because, after all, the origin of life was a historical event that left no direct physical record. However, based on indirect evidence in both the geological record and the phylogenetic record of evolutionary history on earth, it is possible to reconstruct a rough picture of what life was like before DNA and protein.

Joyce, Gerald F.↗
DOE OSTI2024

Pathway Evolution Through a Bottlenecking-Debottlenecking Strategy and Machine Learning-Aided Flux Balancing

The evolution of pathway enzymes enhances the biosynthesis of high-value chemicals, crucial for pharmaceutical, and agrochemical applications. However, unpredictable evolutionary landscapes of pathway genes often hinder successful evolution. Here, the presence of complex epistasis is identifued within the representative naringenin biosynthetic pathway enzymes, hampering straightforward directed evolution. Subsequently, a biofoundry-assisted strategy is developed for pathway bottlenecking and debottlenecking, enabling the parallel evolution of all pathway enzymes along a predictable evolutionary trajectory in six weeks. This study then utilizes a machine learning model, ProEnsemble, to further balance the pathway by optimizing the transcription of individual genes. The broad applicability of this strategy is demonstrated by constructing an Escherichia coli chassis with evolved and balanced pathway genes, resulting in 3.65 g L -1 naringenin. The optimized naringenin chassis also demonstrates enhanced production of other flavonoids. This approach can be readily adapted for any given number of enzymes in the specific metabolic pathway, paving the way for automated chassis construction in contemporary biofoundries.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2023

Common origin of sterol biosynthesis points to a feeding strategy shift in Neoproterozoic animals

Steranes preserved in sedimentary rocks serve as molecular fossils, which are thought to record the expansion of eukaryote life through the Neoproterozoic Era (~1000-541 Ma). Scientists hypothesize that ancient C 27 steranes originated from cholesterol, the major sterol produced by living red algae and animals. Similarly, C 28 and C 29 steranes are thought to be derived from the sterols of prehistoric fungi, green algae, and other microbial eukaryotes. However, recent work on annelid worms–an advanced group of eumetazoan animals–shows that they are also capable of producing C 28 and C 29 sterols. In this paper, we explore the evolutionary history of the 24-C sterol methyltransferase (smt) gene in animals, which is required to make C 28+ sterols. We find evidence that the smt gene was vertically inherited through animals, suggesting early eumetazoans were capable of C 28+ sterol synthesis. Our molecular clock of the animal smt gene demonstrates that its diversification coincides with the rise of C 28 and C 29 steranes in the Neoproterozoic. This study supports the hypothesis that early eumetazoans were capable of making C 28+ sterols and that many animal lineages independently abandoned its biosynthesis around the end-Neoproterozoic, coinciding with the rise of abundant eukaryotic prey.

59 BASIC BIOLOGICAL SCIENCES↗