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All sources NASA NTRS DOE OSTI

DOE OSTI2025

Tropical Forest Soil Microbiome Modulates Leaf Heat Tolerance More Strongly Under Warming Than Ambient Conditions

ABSTRACT It is unclear how plants respond to increasing temperatures. Leaf heat tolerance (LHT) is often at its upper limit in tropical forests, suggesting that climate change might negatively impact these forests. We hypothesized that intraspecific variation in LHT might be associated with changes in the soil microbiome, which might also respond to climate. We hypothesized that warming would increase LHT through changes in the soil microbiome: we combined an in situ tropical warming experiment with a shade house experiment in Puerto Rico. The shade house experiment consisted of growing seedlings of Guarea guidonia , a dominant forest species, under different soil microbiome treatments (reduced arbuscular mycorrhizal fungi, reduced plant pathogens, reduced microbes, and unaltered) and soil inoculum from the field experiment. Heat tolerance was determined using chlorophyll fluorescence ( F V /F m ) on individual seedlings in the field and on groups of seedlings (per pot) in the shade house. We sequenced soil fungal DNA to analyze the impacts of the treatments on the soil microbiome. In the field, seedlings from ambient temperature plots showed higher F V /F m values under high temperatures (0.648 at 46°C and 0.067 at 52°C) than seedlings from the warming plots (0.535 at 46°C and 0.031 at 52°C). In the shade house, the soil microbiome treatments significantly influenced the fungal community composition and LHT ( T crit and F V /F m ). Reduction in fungal pathogen abundance and diversity altered F V /F m before T 50 for seedlings grown with soil inoculum from the warming plots but after T 50 for seedlings grown with soil inoculum from the ambient plots. Our findings emphasize that the soil microbiome plays an important role in modulating the impacts of climate change on plants. Understanding and harnessing this relationship might be vital for mitigating the effects of warming on forests, emphasizing the need for further research on microbial responses to climate change.

Hernandes Villani, Gabriela [Department of Plant B↗

DOE OSTI2023

cotH Genes Are Necessary for Normal Spore Formation and Virulence in Mucor lusitanicus

Mucormycosis is an invasive fungal infection caused by certain members of the fungal order of Mucorales. The species most frequently identified as the etiological agents of mucormycosis belong to the genera Rhizopus , Lichtheimia , and Mucor . The frequency of systemic mucormycosis has been increasing, mainly because of increasing numbers of susceptible patients. Furthermore, Mucorales display intrinsic resistance to the majority of routinely used antifungal agents (e.g., echinocandins and short-tailed azoles), which limits the number of possible therapeutic options. All the above-mentioned issues urge the improvement of molecular identification methods and the discovery of new antifungal targets and strategies. Spore coat proteins (CotH) constitute a kinase family present in many pathogenic bacteria and fungi and participate in the spore formation in these organisms. Moreover, some of them can act as virulence factors being receptors of the human GRP78 protein during Rhizopus delemar-induced mucormycosis. We identified 17 cotH -like genes in the Mucor lusitanicus genome database. Successful disruption of five cotH genes in Mucor was performed using the CRISPR-Cas9 system. The CotH3 and CotH4 proteins play a role in adaptation to different temperatures as well as in developing the cell wall structure. We also show CotH4 protein is involved in spore wall formation by affecting the total chitin content and, thus, the composition of the spore wall. The role of CotH3 and CotH4 proteins in virulence was confirmed in two invertebrate models and a diabetic ketoacidosis (DKA) mouse model.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRSDate not supplied

Restricted by A Historical Review of Strategies and Organization for Restricted Earth Return of Samples from NASA Planetary Missions

Return of samples from the Moon via the Apollo 11, 12 and 14 missions represented NASA's first attempts into conducting what is now known as Restricted Earth Return. When Apollo returned samples from the moon, there were few of the agencies, legal and organizational structures that exist now. A half a century later, the U.S system has seen changes in legal and organizational structures with the appearance of different agencies and legal requirements. During the Apollo era, U.S. legal and organizational structures, assessed threats to the Earth’s biosphere with a priority towards the risks of effects from extraterrestrial pathogens on humans, though the guiding document, the Baylor Protocol, also considered animal and plant models. This presentation focuses on a review of two main questions: Did the return of samples from the Moon happen at a “sweet spot” in time, where the number of requirements and conservatism was commensurate with the scientific knowns and unknowns? Could the emphasis of risk mitigation on human pathogens during the return of extraterrestrial samples be more about human solipsism, leaving us with a blind spot to sources of pathogens, such as fungi, which could lead to an impact to our biosphere, and we humans, via our food chains and agricultural pathways?

planetary protection↗

DOE OSTI2025

Phylogenetic and ecological drivers of the avian lung mycobiome and its potentially pathogenic component

Vertebrate lungs contain diverse microbial communities, but little is known about the drivers of community composition or consequences for health. Microbiome assembly by processes such as dispersal, coevolution, and host-switching can be probed with comparative surveys; however, few studies exist for lung microbiomes, particularly for the fungal component, the mycobiome. Distinguishing among fungal taxa that are generalist or specialist symbionts, potential pathogens, or incidentally inhaled spores is urgent because of potential for emerging diseases. Here, we characterize the avian lung mycobiome and test the relative influences of environment, phylogeny, and functional traits. We used metabarcoding and culturing from 195 lung samples representing 32 bird species across 20 families. We identified 526 fungal taxa as estimated by distinct sequence types (zOTUs) including many opportunistic pathogens. These were predominantly from the phylum Ascomycota (79%) followed by Basidiomycota (16%) and Mucoromycota (5%). Yeast and yeast-like taxa (Malassezia, Filobasidium, Saccharomyces, Meyerozyma, and Aureobasidium) and filamentous fungi (Cladosporium, Alternaria, Neurospora, Fusarium, and Aspergillus) were abundant. Lung mycobiomes were strongly shaped by environmental exposure, and further modulated by host identity, traits, and phylogenetic affinities. Our results implicate migratory bird species as potential vectors for long-distance dispersal of opportunistically pathogenic fungi.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Genetic time traveling: sequencing old herbarium specimens, including the oldest herbarium specimen sequenced from kingdom Fungi, reveals the population structure of an agriculturally significant rust

Summary Sequencing herbarium specimens can be instrumental in answering ecological, evolutionary, and taxonomic inquiries. We developed a protocol for sequencing herbarium specimens of rust fungi (Pucciniales) and proceeded to sequence specimens ranging from 4 to 211 yr old from five different genera. We then obtained sequences from an economically important biological control agent, Puccinia suaveolens , to highlight the potential of sequencing herbarium specimens in an ecological sense and to evaluate the following hypotheses: (1) The population structure of a plant pathogen changes over time, and (2) introduced pathogens are more diverse in their native range. Our efforts resulted in sequences from 87 herbarium specimens that revealed a high level of diversity with a population structure that exhibited spatial–temporal patterns. The specimens sequenced from Europe showed more diversity than the ones from North America, uncovering an invasion pattern likely related to its European native host in North America. Additionally, to the best of our knowledge, the specimen from France collected in c. 1811 is the oldest herbarium specimen sequenced from kingdom Fungi. In conclusion, sequencing old herbarium specimens is an important tool that can be extrapolated to better understand plant–microbe evolution and to evaluate old type specimens to solidify the taxonomy of plant pathogenic fungi.

Plant Sciences↗

NASA NTRS2019

Plant Microbiomes May Provide Vital Information to Plant Success

Plant associated microbiomes, the rhizosphere and phyllosphere, are composed of communities of bacteria and fungi that may be mutualistic or pathogenic. These communities have the potential to influence plant health and development and can affect plant growth. Crop plants are being investigated as a fresh and safe supplement to astronauts’ diet and it is critical to understand and characterize these microbial communities. Multi-species crops, Mizuna mustard (Brassica rapa var japonica), ‘Outredgeous’ red romaine lettuce (Lactuca sativa), and Waldman’s Green lettuce (Lactuca sativa) were grown in two Veggie units on the International Space Station (ISS) for three grow outs in various combinations of plant types. Upon harvest, plant and pillow samples were frozen and returned to Earth for analysis. Bacterial and fungal community analyses for plant leaf and root, as well as pillow components, wick and media, were completed using next generation sequencing with the goal of surveying the composition of the entire community and identifying any potential pathogens. Bacteria were identified using the 16S rRNA gene whereas, fungi were identified with the internal transcribed spacer (ITS). The community composition for these three crops was compared between crop types and between plant tissue types. It is vital to mission success for the short term and long term to add nutritious, safe to eat vegetables providing a supplement to the crew members’ dietary requirements as well as to develop planning for deep space missions as we reach for the moon and on to Mars. Veggie technology validation tests were supported by NASA’s Space Biology Program.

Khodadad, Christina L.↗

NASA NTRS1976

The Identification of Scientific Programs to Utilize the Space Environment

A program to identify and develop ideas for scientific experimentation on the long duration exposure facility (LDEF) was completed. Four research proposals were developed: (1) Ultra pure germanium gamma ray radiation detectors in the space environment, intended to develop and demonstrate an X-ray and gamma-ray spectroscopy system incorporating a temperature cyclable high-purity germanium detector and diode heat pipe cryogenic system for cooling, (2) growth, morphogenesis and metabolism of plant embryos in the zero-gravity environment, to investigate if the space environment induces mutations in the embryogenic cells so that mutants of commercial significance with desirable attributes may be obtained, (3) effect of zero gravity on the growth and pathogenicity of selected zoopathic fungi. It is possible that new kinds of treatment for candidiasis, and tichophytosis could eventuate from the results of the proposed studies, and (4) importance of gravity to survival strategies of small animals. Gravitational effects may be direct or mediate the selection of genetic variants that are preadapted to weightlessness.

Kulacki, F. A.↗

DOE OSTI2021

Global Diversity and Biogeography of the Zostera marina Mycobiome

Seagrasses are marine flowering plants that provide critical ecosystem services in coastal environments worldwide. Marine fungi are often overlooked in microbiome and seagrass studies, despite terrestrial fungi having critical functional roles as decomposers, pathogens, or endophytes in global ecosystems. Here, we characterize the distribution of fungi associated with the seagrass Zostera marina, using leaves, roots, and rhizosphere sediment from 16 locations across its full biogeographic range. Using high-throughput sequencing of the ribosomal internal transcribed spacer (ITS) region and 18S rRNA gene, we first measured fungal community composition and diversity. We then tested hypotheses of neutral community assembly theory and the degree to which deviations suggested that amplicon sequence variants (ASVs) were plant selected or dispersal limited. Finally, we identified a core mycobiome and investigated the global distribution of differentially abundant ASVs. We found that the fungal community is significantly different between sites and that the leaf mycobiome follows a weak but significant pattern of distance decay in the Pacific Ocean. Generally, there was evidence for both deterministic and stochastic factors contributing to community assembly of the mycobiome, with most taxa assembling through stochastic processes. The Z. marina core leaf and root mycobiomes were dominated by unclassified Sordariomycetes spp., unclassified Chytridiomycota lineages (including Lobulomycetaceae spp.), unclassified Capnodiales spp., and Saccharomyces sp. It is clear from the many unclassified fungal ASVs and fungal functional guilds that knowledge of marine fungi is still rudimentary. Further studies characterizing seagrass-associated fungi are needed to understand the roles of these microorganisms generally and when associated with seagrasses. Fungi have important functional roles when associated with land plants, yet very little is known about the roles of fungi associated with marine plants, like seagrasses. In this study, we report the results of a global effort to characterize the fungi associated with the seagrass Zostera marina across its full biogeographic range. Although we defined a putative global core fungal community, it is apparent from the many fungal sequences and predicted functional guilds that had no matches to existing databases that general knowledge of seagrass-associated fungi and marine fungi is lacking. This work serves as an important foundational step toward future work investigating the functional ramifications of fungi in the marine ecosystem.

ITS2↗

DOE OSTI2024

Comparative genomics and stable isotope analysis reveal the saprotrophic-pathogenic lifestyle of a neotropical fungus

In terrestrial forested ecosystems, fungi may interact with trees in at least three distinct ways: (i) associated with roots as symbionts; (ii) as pathogens in roots, trunks, leaves, flowers, and fruits; or (iii) decomposing dead tree tissues on soil or even on dead tissues in living trees. Distinguishing the latter two nutrition modes is rather difficult in Hymenochaetaceae (Basidiomycota) species. Herein, we have used an integrative approach of comparative genomics, stable isotopes, host tree association, and bioclimatic data to investigate the lifestyle ecology of the scarcely known neotropical genus Phellinotus, focusing on the unique species Phellinotus piptadeniae. This species is strongly associated with living Piptadenia gonoacantha (Fabaceae) trees in the Atlantic Forest domain on a relatively high precipitation gradient. Phylogenomics resolved P. piptadeniae in a clade that also includes both plant pathogens and typical wood saprotrophs. Furthermore, both genome-predicted Carbohydrate-Active Enzymes (CAZy) and stable isotopes (δ 13 C and δ 15 N) revealed a rather flexible lifestyle for the species. Altogether, our findings suggest that P. piptadeniae has been undergoing a pathotrophic specialization in a particular tree species while maintaining all the metabolic repertoire of a wood saprothroph.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species

Not Available

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2022

Phylogenomics and Comparative Genomics Highlight Specific Genetic Features in Ganoderma Species

The Ganoderma species in Polyporales are ecologically and economically relevant wood decayers used in traditional medicine, but their genomic traits are still poorly documented. In the present study, we carried out a phylogenomic and comparative genomic analyses to better understand the genetic blueprint of this fungal lineage. We investigated seven Ganoderma genomes, including three new genomes, G. australe, G. leucocontextum, and G. lingzhi. The size of the newly sequenced genomes ranged from 60.34 to 84.27 Mb and they encoded 15,007 to 20,460 genes. A total of 58 species, including 40 white-rot fungi, 11 brown-rot fungi, four ectomycorrhizal fungi, one endophyte fungus, and two pathogens in Basidiomycota, were used for phylogenomic analyses based on 143 single-copy genes. It confirmed that Ganoderma species belong to the core polyporoid clade. Comparing to the other selected species, the genomes of the Ganoderma species encoded a larger set of genes involved in terpene metabolism and coding for secreted proteins (CAZymes, lipases, proteases and SSPs). Of note, G. australe has the largest genome size with no obvious genome wide duplication, but showed transposable elements (TEs) expansion and the largest set of terpene gene clusters, suggesting a high ability to produce terpenoids for medicinal treatment. G. australe also encoded the largest set of proteins containing domains for cytochrome P450s, heterokaryon incompatibility and major facilitator families. Besides, the size of G. australe secretome is the largest, including CAZymes (AA9, GH18, A01A), proteases G01, and lipases GGGX, which may enhance the catabolism of cell wall carbohydrates, proteins, and fats during hosts colonization. The current genomic resource will be used to develop further biotechnology and medicinal applications, together with ecological studies of the Ganoderma species.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS1973

The examination of urine samples for pathogenic microbes by the luciferase assay for ATP. 1: The effect of the presence of fungi, fungal like bacteria and kidney cells in urine samples

A method for accurately determining urinary tract infections in man is introduced. The method is based on adenosine triphosphate (ATP) concentration in urine samples after removing nonbacterial ATP. Adenosine triphosphate concentration is measured from the bioluminescent reaction of luciferase when mixed with ATP. An examination was also made of the effectiveness of rupturing agents on monkey kidney cells Candia albicans, a Rhodotorula species, and a Streptomyces species in determining whether these cells could contribute ATP to the bacterial ATP value of a urine sample.

Bush, V. N.↗

NASA NTRS1992

Altered immunological response in mice subjected to stress and exposed to fungal spores

Space flight and related factors such as stress appear to have an adverse effect on astronauts' immune systems. The presence of potentially pathogenic microbes including several genera of fungi reported from spacecraft environment may be a cause of concern in such situations. In order to study the role of such organisms in causing opportunistic or allergic diseases in crewmembers, we have tried to develop an animal model. BALB/c mice were suspended upside down for varying periods of time to induce stress, and their lymphocyte functions were evaluated. These studies indicate that the stress resulted in lowered mitogen induced lymphocyte stimulation as represented by 3H-thymidine uptake. We have also studied the ability of these animals to respond to Aspergillus fumigatus spores. The results of the study clearly demonstrate a definite down-regulation in T-cell proliferation and a higher incidence of infection with A. fumigatus.

Kurup, Viswanath P.↗

DOE OSTI2023

Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil

Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km 2 ) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes—urbanization and forest edge creation—on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new “suites” of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction—including increased greenhouse gas production—in temperate forest regions that are subsumed by urban expansion, both now and in the future.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metabolism might facilitate symbioses with phylogenetically diverse hosts. Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to the breadth of symbiotic interactions and ecological roles. All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition. Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. Altogether, our results provide new evidence that SMGCs may facilitate symbiosis with phylogenetically diverse hosts, highlighting the importance of microbial symbioses to drive fungal metabolic diversity.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2020

The cytochrome bc 1 complex as an antipathogenic target

The cytochrome bc 1 complex is a key component of the mitochondrial respiratory chains of many eukaryotic microorganisms that are pathogenic for plants or humans, such as fungi responsible for crop diseases and Plasmodium falciparum, which causes human malaria. Cytochrome bc 1 is an enzyme that contains two (ubi)quinone/quinol-binding sites, which can be exploited for the development of fungicidal and chemotherapeutic agents. In this article, we review recent progress in determination of the structure and mechanism of action of cytochrome bc 1 , and the associated development of antimicrobial agents (and associated resistance mechanisms) targeting its activity.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Major proliferation of transposable elements shaped the genome of the soybean rust pathogen Phakopsora pachyrhizi

With >7000 species the order of rust fungi has a disproportionately large impact on agriculture, horticulture, forestry and foreign ecosystems. The infectious spores are typically dikaryotic, a feature unique to fungi in which two haploid nuclei reside in the same cell. A key example is Phakopsora pachyrhizi, the causal agent of Asian soybean rust disease, one of the world’s most economically damaging agricultural diseases. Despite P. pachyrhizi’s impact, the exceptional size and complexity of its genome prevented generation of an accurate genome assembly. Here, we sequence three independent P. pachyrhizi genomes and uncover a genome up to 1.25 Gb comprising two haplotypes with a transposable element (TE) content of ~93%. We study the incursion and dominant impact of these TEs on the genome and show how they have a key impact on various processes such as host range adaptation, stress responses and genetic plasticity.

59 BASIC BIOLOGICAL SCIENCES↗

NASA NTRS2019

Leafy Greens Grown on the International Space Station May Provide a Nutritious Supplement to Astronauts' Diet

Supplemental safe food production has been an essential goal of NASA to meet the nutritional needs of astronauts on the International Space Station (ISS) as well as for future long duration missions to the moon and beyond. Food crops grown in space experience different environmental conditions than plants grown on Earth (i.e. microgravity and spaceflight physical sciences impacts). To test the growth methods and effects of the space environment, red romaine lettuce Lactuca sativa cv. 'Outredgeous', was grown in Veggie plant growth chambers on the ISS. Microbiological food safety of the plants grown on the ISS was determined by heterotrophic plate counts to assess total microbial load for bacteria and fungi as well as screening for specific pathogens and isolate identification. Molecular characterization was completed using Next Generation Sequencing (NGS) to provide valuable information on the taxonomic composition and community structure of the plant microbiome. Chemical analyses of plant tissue were conducted to understand spaceflight-induced changes in key elements in the space diet, phenolics, anthocyanin levels, and Oxygen radical absorbance capacity (ORAC), a measure of antioxidant capacity. Three growth tests of red romaine lettuce were completed on ISS, VEG-01A, VEG-01B, and VEG-03A. Plants were harvested using two harvest methods, either a single terminal harvest (after 33 days) or cut-and-come-again repetitive harvesting (64 days total growth). Ground controls were grown simultaneously with a delay to accommodate condition monitoring and replication. A comparison of the plant tissue returned to Earth showed leaves from the second grow-out had significantly higher bacterial counts than the preceding or subsequent growth test or any of the ground controls. Fungal counts were significantly higher on the final cut-and-come-again harvest of the third grow out. None of the potential foodborne pathogens that were screened for were detected. Bacterial and fungal isolate identification and community characterization indicated similar diversity between VEG-01A and VEG-01B growth tests, however, there appeared to be subtle differences in diversity and distribution among the three growth tests. Chemical analysis of plant tissue revealed significant variation in a few elemental data, but variation in levels of phenolics, anthocyanins, and ORAC was not significantly different. This study indicated that leafy vegetable crops could safely provide an edible supplement to astronauts' diet, and our analysis provided baseline data for continual operation of the Veggie plant growth units on ISS. This research was funded by NASA's space biology program.

Food Production↗