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NASA NTRS1989

The evolution of ecological tolerance in prokaryotes

The ecological ranges of Archaeobacteria and Eubacteria are constrained by a requirement for liquid water and the physico-chemical stability limits of biomolecules, but within this broad envelope, prokaryotes have evolved adaptations that permit them to tolerate a remarkable spectrum of habitats. Laboratory experiments indicate that prokaryotes can adapt rapidly to novel environmental conditions, yet geological studies suggest early diversification and long-term stasis within the prokaryotic kingdoms. These apparently contradictory perspectives can be reconciled by understanding that, in general, rates and patterns of prokaryotic evolution reflect the developmental history of the Earth's surface environments. Our understanding of modern microbial ecology provides a lens through which our accumulating knowledge of physiology, molecular phylogeny and the Earth's history can be integrated and focussed on the phenomenon of prokaryotic evolution.

NASA Discipline Number 52-30↗

DOE OSTI2022

Cross-kingdom expression of synthetic genetic elements promotes discovery of metabolites in the human microbiome

Small molecules encoded by biosynthetic pathways mediate cross-species interactions and harbor untapped potential, which has provided valuable compounds for medicine and biotechnology. Since studying biosynthetic gene clusters in their native context is often difficult, alternative efforts rely on heterologous expression, which is limited by host-specific metabolic capacity and regulation. Here, in this work, we describe a computational-experimental technology to redesign genes and their regulatory regions with hybrid elements for cross-species expression in Gram-negative and -positive bacteria and eukaryotes, decoupling biosynthetic capacity from host-range constraints to activate silenced pathways. These synthetic genetic elements enabled the discovery of a class of microbiome-derived nucleotide metabolites—tyrocitabines—from Lactobacillus iners. Tyrocitabines feature a remarkable orthoester-phosphate, inhibit translational activity, and invoke unexpected biosynthetic machinery, including a class of “Amadori synthases” and “abortive” tRNA synthetases. Our approach establishes a general strategy for the redesign, expression, mobilization, and characterization of genetic elements in diverse organisms and communities.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2025

A red algal polysaccharide influences the multicellular development of the choanoflagellate Salpingoeca rosetta

The choanoflagellate Salpingoeca rosetta exemplifies the capacity of marine microeukaryotes to integrate environmental cues into their life histories. Some of the cues that S. rosetta detects are lipids from their bacterial prey that induce the development of multicellular colonies called rosettes. In the aquatic environments where S. rosetta would encounter bacterial cues, microbial communities gain refuge and food from algae. For example, microbes in coastal environments benefit from macroalgae that annually release ∼10 14 g of carbon, primarily in the form of polysaccharides that comprise ∼80% of dissolved organic carbon in surface waters. Despite the ecological impact of algae and historical descriptions of choanoflagellates attached to algae, the influence of algae on choanoflagellate life history transitions has remained unexplored. Here, we report that porphyran, a polysaccharide produced by the red macroalga Porphyra umbilicalis, induces multicellular development in S. rosetta. We first noticed this response when S. rosetta formed multicellular rosette colonies while growing in media prepared from P. umbilicalis, even though rosette-inducing bacteria were absent. By biochemically purifying extracts of P. umbilicalis, we identified porphyran as the rosette-inducing factor. This response provides a biochemical insight that indicates algal polysaccharides may serve as cues to mediate associations between choanoflagellates and algae. Moreover, this observation complements evidence from environmental and geochemical studies that show the impact that algae have exerted on the ecology and evolution of eukaryotes, including a rise in algal productivity during the origin of animals, the closest living relatives of choanoflagellates.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS1990

Kingdom Animalia: the zoological malaise from a microbial perspective

Pain and cognitive dissonance abounds amongst biologists: the plant-animal, botany-zoology wound has nearly healed and the new gash--revealed by department and budget reorganizations--is "molecular" vs. "organismic" biology. Here I contend that resolution of these tensions within zoology requires that an autopoietic-gaian view replace a mechanical-neodarwinian perspective; in the interest of brevity and since many points have been discussed elsewhere, rather than develop detailed arguments I must make staccato statements and refer to a burgeoning literature. The first central concept is that animals, all organisms developing from blastular embryos, evolved from single protist cells that were unable to reproduce their undulipodia. The second points to the usefulness of recognizing the analogy between cyclically established symbioses and meiotic sexuality.

NASA Program Exobiology↗

NASA NTRS1999

Post-Viking microbiology: new approaches, new data, new insights

In the 20 years since the Viking experiments, major advances have been made in the areas of microbial systematics, microbial metabolism, microbial survival capacity, and the definition of environments on earth, suggesting that life is more versatile and tenacious than was previously appreciated. Almost all niches on earth which have available energy, and which are compatible with the chemistry of carbon-carbon bonds, are known to be inhabited by bacteria. The oldest known bacteria on earth apparently evolved soon after the formation of the planet, and are heat loving, hydrogen and/or sulfur metabolizing forms. Among the two microbial domains (kingdoms) is a great deal of metabolic diversity, with members of these forms being able to grow on almost any known energy source, organic or inorganic, and to utilize an impressive array of electron acceptors for anaerobic respiration. Both hydrothermal environments and the deep subsurface environments have been shown to support large populations of bacteria, growing on energy supplied by geothermal energy, thus isolating these ecosystems from the rest of the global biogeochemical cycles. This knowledge, coupled with new insights into the history of the solar system, allow one to speculate on possible evolution and survival of life forms on Mars.

Review↗

DOE OSTI2021

Expanding standards in viromics: in silico evaluation of dsDNA viral genome identification, classification, and auxiliary metabolic gene curation

Viruses influence global patterns of microbial diversity and nutrient cycles. Though viral metagenomics (viromics), specifically targeting dsDNA viruses, has been critical for revealing viral roles across diverse ecosystems, its analyses differ in many ways from those used for microbes. To date, viromics benchmarking has covered read pre-processing, assembly, relative abundance, read mapping thresholds and diversity estimation, but other steps would benefit from benchmarking and standardization. Here we use in silico-generated datasets and an extensive literature survey to evaluate and highlight how dataset composition (i.e., viromes vs bulk metagenomes) and assembly fragmentation impact (i) viral contig identification tool, (ii) virus taxonomic classification, and (iii) identification and curation of auxiliary metabolic genes (AMGs). The in silico benchmarking of five commonly used virus identification tools show that gene-content-based tools consistently performed well for long (≥3 kbp) contigs, while k -mer- and blast-based tools were uniquely able to detect viruses from short (≤3 kbp) contigs. Notably, however, the performance increase of k -mer- and blast-based tools for short contigs was obtained at the cost of increased false positives (sometimes up to ~5% for virome and ~75% bulk samples), particularly when eukaryotic or mobile genetic element sequences were included in the test datasets. Furthermore, for viral classification, variously sized genome fragments were assessed using gene-sharing network analytics to quantify drop-offs in taxonomic assignments, which revealed correct assignations ranging from ~95% (whole genomes) down to ~80% (3 kbp sized genome fragments). A similar trend was also observed for other viral classification tools such as VPF-class, ViPTree and VIRIDIC, suggesting that caution is warranted when classifying short genome fragments and not full genomes. Finally, we highlight how fragmented assemblies can lead to erroneous identification of AMGs and outline a best-practices workflow to curate candidate AMGs in viral genomes assembled from metagenomes. Together, these benchmarking experiments and annotation guidelines should aid researchers seeking to best detect, classify, and characterize the myriad viruses ‘hidden’ in diverse sequence datasets.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

The role of zinc in the adaptive evolution of polar phytoplankton

Zinc is an essential trace metal for oceanic primary producers with the highest concentrations in polar oceans. However, its role in the biological functioning and adaptive evolution of polar phytoplankton remains enigmatic. Here, we have applied a combination of evolutionary genomics, quantitative proteomics, co-expression analyses and cellular physiology to suggest that model polar phytoplankton species have a higher demand for zinc because of elevated cellular levels of zinc-binding proteins. We propose that adaptive expansion of regulatory zinc-finger protein families, co-expanded and co-expressed zinc-binding proteins families involved in photosynthesis and growth in these microalgal species and their natural communities were identified to be responsible for the higher zinc demand. The expression of their encoding genes in eukaryotic phytoplankton metatranscriptomes from pole-to-pole was identified to correlate not only with dissolved zinc concentrations in the upper ocean but also with temperature, suggesting that environmental conditions of polar oceans are responsible for an increased demand of zinc. Furthermore, these results suggest that zinc plays an important role in supporting photosynthetic growth in eukaryotic polar phytoplankton and that this has been critical for algal colonization of low-temperature polar oceans.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Effects of water recirculation on microalgae assemblage and corresponding sustainability of the photobioreactor cultivation system

An algae photobioreactor (APB) was used to determine the effect of water recirculation on the growth of algal assemblage. CO 2 in the flue gas from a power plant was the carbon source. Boiler water was used as the source water. The results showed that microalgae cultivation under recirculation conditions was stable over a period of four months. Biomass productivities during the 1st through 4th months of recirculation (0.26, 0.23, 0.20, and 0.18 g L –1 d –1 , respectively) were not significantly different than freshwater (0.22 g L –1 d –1 ). Furthermore, the relationship between eukaryotic and bacterial domains in the assemblage remained consistent throughout the four months of recirculation (80.7, 87.1, 83.1, and 82.1%, respectively, and 19.2, 12.8, 16.9, and 17.8%, respectively). This was not significantly different than the abundance of each domain in the control freshwater cultivation (83.7% eukaryotic and 16.2% bacterial). A 1 m 3 photobioreactor was then envisioned for a mass, energy, and exergy analysis to evaluate the water recirculation on sustainability of the culture system. The mass balance analysis concluded that 98% reduction in water usage, 25% reduction in nitrogen, and 12.5% reduction in phosphorus could be achieved during cultivation operating under recirculation for one year, while maintaining biomass productivity of 1.2 kg wet algal biomass and sequestration of 0.4 kg CO 2 per day. Furthermore, the exergy balance analysis concluded that without considering solar irradiation, the culture with water recirculation greatly enhanced the rational exergy efficiency, which represents a more sustainable cultivation system for CO 2 capture and utilization.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2023

Virus Infection of Phytoplankton Increases Average Molar Mass and Reduces Hygroscopicity of Aerosolized Organic Matter

Viral infection of phytoplankton is a pervasive mechanism of cell death and bloom termination, which leads to the production of dissolved and colloidal organic matter that can be aerosolized into the atmosphere. Earth-observing satellites can track the growth and death of phytoplankton blooms on weekly time scales but the impact of viral infection on the cloud forming potential of associated aerosols is largely unknown. Here, we determine the influence of viral-derived organic matter, purified viruses, and marine hydrogels on the cloud condensation nuclei activity of their aerosolized solutions, compared to organic exudates from healthy phytoplankton. Dissolved organic material derived from exponentially growing and infected cells of well-characterized eukaryotic phytoplankton host-virus systems, including viruses from diatoms, coccolithophores and chlorophytes, was concentrated, desalted, and nebulized to form aerosol particles composed of primarily of organic matter. Aerosols from infected phytoplankton cultures resulted in an increase in critical activation diameter and average molar mass in three out of five combinations evaluated, along with a decrease in organic kappa (hygroscopicity) compared to healthy cultures and seawater controls. The infected samples also displayed evidence of increased surface tension depression at realistic cloud water vapor supersaturations. Amending the samples with xanthan gum to simulate marine hydrogels increased variability in organic kappa and surface tension in aerosols with high organic to salt ratios. Our findings suggest that the pulses of increased dissolved organic matter associated with viral infection in surface waters may increase the molar mass of dissolved organic compounds relative to surface waters occupied by healthy phytoplankton or low phytoplankton biomass.

Atmospheric science↗

DOE OSTI2024

Distinct and rich assemblages of giant viruses in Arctic and Antarctic lakes

Giant viruses (GVs) are key players in ecosystem functioning, biogeochemistry, and eukaryotic genome evolution. GV diversity and abundance in aquatic systems can exceed that of prokaryotes, but their diversity and ecology in lakes, especially polar ones, remain poorly understood. We conducted a comprehensive survey and meta-analysis of GV diversity across 20 lakes, spanning polar to temperate regions, combining our extensive lake metagenome database from the Canadian Arctic and subarctic with publicly available datasets. Leveraging a novel GV genome identification tool, we identified 3304 GV metagenome-assembled genomes, revealing lakes as untapped GV reservoirs. Phylogenomic analysis highlighted their dispersion across all Nucleocytoviricota orders. Strong GV population endemism emerged between lakes from similar regions and biomes (Antarctic and Arctic), but a polar/temperate barrier in lacustrine GV populations and differences in their gene content could be observed. Our study establishes a robust genomic reference for future investigations into lacustrine GV ecology in fast changing polar environments.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2012

Purifying, Separating, and Concentrating Cells From a Sample Low in Biomass

Frequently there is an inability to process and analyze samples of low biomass due to limiting amounts of relevant biomaterial in the sample. Furthermore, molecular biological protocols geared towards increasing the density of recovered cells and biomolecules of interest, by their very nature, also concentrate unwanted inhibitory humic acids and other particulates that have an adversarial effect on downstream analysis. A novel and robust fluorescence-activated cell-sorting (FACS)-based technology has been developed for purifying (removing cells from sampling matrices), separating (based on size, density, morphology), and concentrating cells (spores, prokaryotic, eukaryotic) from a sample low in biomass. The technology capitalizes on fluorescent cell-sorting technologies to purify and concentrate bacterial cells from a low-biomass, high-volume sample. Over the past decade, cell-sorting detection systems have undergone enhancements and increased sensitivity, making bacterial cell sorting a feasible concept. Although there are many unknown limitations with regard to the applicability of this technology to environmental samples (smaller cells, few cells, mixed populations), dogmatic principles support the theoretical effectiveness of this technique upon thorough testing and proper optimization. Furthermore, the pilot study from which this report is based proved effective and demonstrated this technology capable of sorting and concentrating bacterial endospore and bacterial cells of varying size and morphology. Two commercial off-the-shelf bacterial counting kits were used to optimize a bacterial stain/dye FACS protocol. A LIVE/DEAD BacLight Viability and Counting Kit was used to distinguish between the live and dead cells. A Bacterial Counting Kit comprising SYTO BC (mixture of SYTO dyes) was employed as a broad-spectrum bacterial counting agent. Optimization using epifluorescence microscopy was performed with these two dye/stains. This refined protocol was further validated using varying ratios and mixtures of cells to ensure homogenous staining compared to that of individual cells, and were utilized for flow analyzer and FACS labeling. This technology focuses on the purification and concentration of cells from low-biomass spacecraft assembly facility samples. Currently, purification and concentration of low-biomass samples plague planetary protection downstream analyses. Having a capability to use flow cytometry to concentrate cells out of low-biomass, high-volume spacecraft/ facility sample extracts will be of extreme benefit to the fields of planetary protection and astrobiology. Successful research and development of this novel methodology will significantly increase the knowledge base for designing more effective cleaning protocols, and ultimately lead to a more empirical and true account of the microbial diversity present on spacecraft surfaces. Refined cleaning and an enhanced ability to resolve microbial diversity may decrease the overall cost of spacecraft assembly and/or provide a means to begin to assess challenging planetary protection missions.

Benardini, James N.↗

DOE OSTI2025

Seasonal Host Shifts for Legionella Within an Industrial Water‐Cooling System

Legionella is a genus of environmental bacteria containing pathogenic species such as Legionella pneumophila that are responsible for Legionnaires' disease, a potentially fatal respiratory infection. Disease aetiology can involve Legionella replication intracellularly within protists and this study aimed to characterise the Legionella -protist relationship to develop novel outbreak prevention targets. Water and sediment samples were collected from a water-cooling tower in South Carolina over a 6-month period. Concomitantly, multiple environmental parameters were recorded. Bacterial and eukaryotic communities were characterised using 16S rRNA gene V4 region and a 252 bp fragment of 18S rRNA gene, respectively. Co-occurrence network analyses were performed to elucidate Legionella -protist correlations through time. We found that Legionella correlated with different protists as the seasons progressed. Acanthamoeba correlated with Legionella in early spring followed by Vannella and Korotnevella in late spring and early summer, and were joined by Echinamoeba in mid-summer. Vannella and Acanthamoeba are known potential hosts for Legionella , while Korotnevella is a potential undocumented host. Of the environmental parameters, temperature showed strong correlation with protists genera, suggesting that Legionella abundance was driven by temperature-dependent protist availability. Our results highlight ecological shifts that are associated with elevated Legionella levels, which offers potential targets to help predict and prevent disease outbreaks.

microbial communities↗

DOE OSTI2025

Global Archaeal Diversity Revealed Through Massive Data Integration: Uncovering Just Tip of Iceberg

The domain of Archaea has gathered significant interest for its ecological and biotechnological potential and its role in helping us to understand the evolutionary history of Eukaryotes. In comparison to the bacterial domain, the number of adequately described members in Archaea is relatively low, with less than 1000 species described. It is not clear whether this is solely due to the cultivation difficulty of its members or, indeed, the domain is characterized by evolutionary constraints that keep the number of species relatively low. Based on molecular evidence that bypasses the difficulties of formal cultivation and characterization, several novel clades have been proposed, enabling insights into their metabolism and physiology. Given the extent of global sampling and sequencing efforts, it is now possible and meaningful to question the magnitude of global archaeal diversity based on molecular evidence. To do so, we extracted all sequences classified as Archaea from 500 thousand amplicon samples available in public repositories. After processing through our highly conservative pipeline, we named this comprehensive resource the ‘Global Archaea Diversity’ (GAD), which encompassed nearly 3 million molecular species clusters at 97% similarity, and organized it into over 500 thousand genera and nearly 100 thousand families. Saline environments have contributed the most to the novel taxa of this previously unseen diversity. The majority of those 16S rRNA gene sequence fragments were verified by matches in metagenomic datasets from IMG/M. These findings reveal a vast and previously overlooked diversity within the Archaea, offering insights into their ecological roles and evolutionary importance while establishing a foundation for the future study and characterization of this intriguing domain of life.

59 BASIC BIOLOGICAL SCIENCES↗