Jana M U'Ren

Interests

Research

Microbial genomics, metagenomics, microbial ecology, phylogenetics, evolutionary biology.

Teaching

Microbial genomics, metagenomics, data analytics, microbial ecology.

Courses

Scholarly Contributions

Journals/Publications

• Arnold, A. E., Harrington, A. H., Huang, Y. L., U'Ren, J. M., Massimo, N. C., Knight-Connoni, V., & Inderbitzin, P. (2021). Coniochaeta elegans sp. nov., Coniochaeta montana sp. nov. and Coniochaeta nivea sp. nov., three new species of endophytes with distinctive morphology and functional traits.. International journal of systematic and evolutionary microbiology, 71(11).
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  A growing interest in fungi that occur within symptom-less plants and lichens (endophytes) has uncovered previously uncharacterized species in diverse biomes worldwide. In many temperate and boreal forests, endophytic (Sacc.) Cooke (, , ) are commonly isolated on standard media, but rarely are characterized. We examined 26 isolates of housed at the Gilbertson Mycological Herbarium. The isolates were collected from healthy photosynthetic tissues of conifers, angiosperms, mosses and lichens in Canada, Sweden and the United States. Their barcode sequences (nuclear ribosomal internal transcribed spacer and 5.8S; ITS rDNA) were ≤97% similar to any documented species available through GenBank. Phylogenetic analyses based on two loci (ITS rDNA and translation elongation factor 1-alpha) indicated that two isolates represented , broadening the ecological niche and geographic range of a species known previously from burned soil in Japan. The remaining 24 endophytes represented three previously undescribed species that we characterize here: sp. nov., sp. nov. and sp. nov. Each has a wide host range, including lichens, bryophytes and vascular plants. sp. nov. and sp. nov. have wide geographic ranges. sp. nov. occurs in the Madrean biome of Arizona (USA), where it is sympatric with the other species described here. All three species display protease, chitinase and cellulase activity . Overall, this study provides insight into the ecological and evolutionary diversity of and suggests that these strains may be amenable for studies of traits relevant to a horizontally transmitted, symbiotic lifestyle.
• Arnold, A. E., Harrington, A. H., Uren, J. M., Oita, S., & Inderbitzin, P. (2021). Two new endophytic species enrich the Coniochaeta endophytica/C. prunicola clade: Coniochaeta lutea sp. nov. and C. palaoa sp. nov. Plant and Fungal Systematics, 66, 66–78.
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  A.E. Arnold, A.H. Harrington, J.M. U'Ren, S. Oita, P. Inderbitzin. 2021. Two new endophytic species enrich the Coniochaeta endophytica/C. prunicola clade: Coniochaeta lutea sp. nov. and C. palaoa sp. nov. Plant and Fungal Systematics 66: 66–78.
• Oita, S., Carey, J., Kline, I., Ibáñez, A., Yang, N., Hom, E. F., Carbone, I., U'Ren, J. M., & Arnold, A. E. (2021). Methodological Approaches Frame Insights into Endophyte Richness and Community Composition. Microbial ecology, 82(1), 21-34.
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  Isolating microbes is vital to study microbiomes, but insights into microbial diversity and ecology can be constrained by recalcitrant or unculturable strains. Culture-free methods (e.g., next-generation sequencing, NGS) have become popular in part because they detect greater richness than culturing alone. Both approaches are used widely to characterize microfungi within healthy leaves (foliar endophytes), but methodological differences among studies can constrain large-scale insights into endophyte ecology. We examined endophytes in a temperate plant community to quantify how certain methodological factors, such as the choice of cultivation media for culturing and storage period after leaf collection, affect inferences regarding endophyte communities; how such effects vary among plant taxa; and how complementary culturing and NGS can be when subsets of the same plant tissue are used for each. We found that endophyte richness and composition from culturing were consistent across five media types. Insights from culturing and NGS were largely robust to differences in storage period (1, 5, and 10 days). Although endophyte richness, composition, and taxonomic diversity identified via culturing vs. NGS differed markedly, both methods revealed host-structured communities. Studies differing only in cultivation media or storage period thus can be compared to estimate endophyte richness, composition, and turnover at scales larger than those of individual studies alone. Our data show that it is likely more important to sample more host species, rather than sampling fewer species more intensively, to quantify endophyte diversity in given locations, with the richest insights into endophyte ecology emerging when culturing and NGS are paired.
• Oita, S., Ibáñez, A., Lutzoni, F., Miadlikowska, J., Geml, J., Lewis, L. A., Hom, E. F., Carbone, I., U'Ren, J. M., & Arnold, A. E. (2021). Climate and seasonality drive the richness and composition of tropical fungal endophytes at a landscape scale. Communications biology, 4(1), 313.
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  Understanding how species-rich communities persist is a foundational question in ecology. In tropical forests, tree diversity is structured by edaphic factors, climate, and biotic interactions, with seasonality playing an essential role at landscape scales: wetter and less seasonal forests typically harbor higher tree diversity than more seasonal forests. We posited that the abiotic factors shaping tree diversity extend to hyperdiverse symbionts in leaves-fungal endophytes-that influence plant health, function, and resilience to stress. Through surveys in forests across Panama that considered climate, seasonality, and covarying biotic factors, we demonstrate that endophyte richness varies negatively with temperature seasonality. Endophyte community structure and taxonomic composition reflect both temperature seasonality and climate (mean annual temperature and precipitation). Overall our findings highlight the vital role of climate-related factors in shaping the hyperdiversity of these important and little-known symbionts of the trees that, in turn, form the foundations of tropical forest biodiversity.
• Ponsero, A. J., Hurwitz, B. L., Magain, N., Miadlikowska, J., Lutzoni, F., & Uren, J. M. (2021). Cyanolichen microbiome contains novel viruses that encode genes to promote microbial metabolism. ISME Communications, 1(56), 1.
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  A.J. Ponsero, B.H. Hurwitz, N. Magain, J. Miadlikowska, F. Lutzoni, J.M. U'Ren. 2021. Cyanolichen microbiome contains novel viruses that encode genes to promote microbial metabolism. ISME Communications 1:56.
• Qu, W., Kithsiri Wijeratne, E. M., Bashyal, B. P., Xu, J., Xu, Y. M., Liu, M. X., Inácio, M. C., Arnold, A. E., U'Ren, J. M., & Leslie Gunatilaka, A. A. (2021). Strobiloscyphones A-F, 6-Isopentylsphaeropsidones and Other Metabolites from sp. AZ0266, a Leaf-Associated Fungus of Douglas Fir. Journal of natural products, 84(9), 2575-2586.
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  Six new 6-isopentylsphaeropsidones, strobiloscyphones A-F (-), and a new hexadecanoic acid, (2,4,6)-8,9-dihydroxy-10-oxohexadeca-2,4,6-trienoic acid (), together with sphaeropsidone () and its known synthetic analogue 5-dehydrosphaeropsidone () were isolated from sp. AZ0266, a fungus inhabiting the leaf litter of Douglas fir (). The structures of - were established on the basis of their high-resolution mass and 1D and 2D NMR spectroscopic data, and their relative and/or absolute configurations were determined by NOE, comparison of experimental and calculated ECD spectra, and application of the modified Mosher's ester method. Of these, strobiloscyphone F () contains a novel highly oxygenated tetracyclic oxireno-octahydrodibenzofuran ring system. Natural products , , and and the semisynthetic analogue derived from exhibited cytotoxic activity, whereas and showed antimicrobial activity. Possible biosynthetic pathways to -, , and are proposed.
• U'Ren, J. M., & Zimmerman, N. B. (2021). Oaks provide new perspective on seed microbiome assembly. The New phytologist, 230(4), 1293-1295.
• Apprill, A., Miller, C. A., Van Cise, A. M., U'Ren, J. M., Leslie, M. S., Weber, L., Baird, R. W., Robbins, J., Landry, S., Bogomolni, A., & Waring, G. (2020). Marine mammal skin microbiotas are influenced by host phylogeny. Royal Society open science, 7(5), 192046.
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  Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai'i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.
• Selbmann, L., Benkő, Z., Coleine, C., de Hoog, S., Donati, C., Druzhinina, I., Emri, T., Ettinger, C. L., Gladfelter, A. S., Gorbushina, A. A., Grigoriev, I. V., Grube, M., Gunde-Cimerman, N., Karányi, Z. Á., Kocsis, B., Kubressoian, T., Miklós, I., Miskei, M., Muggia, L., , Northen, T., et al. (2020). Shed Light in the DaRk LineagES of the Fungal Tree of Life-STRES. Life (Basel, Switzerland), 10(12).
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  The polyphyletic group of black fungi within the Ascomycota (Arthoniomycetes, Dothideomycetes, and Eurotiomycetes) is ubiquitous in natural and anthropogenic habitats. Partly because of their dark, melanin-based pigmentation, black fungi are resistant to stresses including UV- and ionizing-radiation, heat and desiccation, toxic metals, and organic pollutants. Consequently, they are amongst the most stunning extremophiles and poly-extreme-tolerant organisms on Earth. Even though ca. 60 black fungal genomes have been sequenced to date, [mostly in the family Herpotrichiellaceae (Eurotiomycetes)], the class Dothideomycetes that hosts the largest majority of extremophiles has only been sparsely sampled. By sequencing up to 92 species that will become reference genomes, the "Shed light in The daRk lineagES of the fungal tree of life" (STRES) project will cover a broad collection of black fungal diversity spread throughout the Fungal Tree of Life. Interestingly, the STRES project will focus on mostly unsampled genera that display different ecologies and life-styles (e.g., ant- and lichen-associated fungi, rock-inhabiting fungi, etc.). With a resequencing strategy of 10- to 15-fold depth coverage of up to ~550 strains, numerous new reference genomes will be established. To identify metabolites and functional processes, these new genomic resources will be enriched with metabolomics analyses coupled with transcriptomics experiments on selected species under various stress conditions (salinity, dryness, UV radiation, oligotrophy). The data acquired will serve as a reference and foundation for establishing an encyclopedic database for fungal metagenomics as well as the biology, evolution, and ecology of the fungi in extreme environments.
• Xu, Y. M., Arnold, A. E., URen, J. M., Xuan, L. J., Wang, W. Q., & Gunatilaka, A. A. (2020). Teratopyrones A–C, Dimeric Naphtho-γ-Pyrones and other metabolites from Teratosphaeria sp. AK1128, a fungal endophyte of Equisetum arvense. Molecules (Basel, Switzerland), 25(21).
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  Bioassay-guided fractionation of a cytotoxic extract derived from a solid potato dextrose agar (PDA) culture of sp. AK1128, a fungal endophyte of , afforded three new naphtho-γ-pyrone dimers, teratopyrones A-C (-), together with five known naphtho-γ-pyrones, aurasperone B (), aurasperone C (), aurasperone F (), nigerasperone A (), and fonsecin B (), and two known diketopiperazines, asperazine () and isorugulosuvine (). The structures of - were determined on the basis of their spectroscopic data. Cytotoxicity assay revealed that nigerasperone A () was moderately active against the cancer cell lines PC-3M (human metastatic prostate cancer), NCI-H460 (human non-small cell lung cancer), SF-268 (human CNS glioma), and MCF-7 (human breast cancer), with ICs ranging from 2.37 to 4.12 μM while other metabolites exhibited no cytotoxic activity up to a concentration of 5.0 μM.
• Carbone, I., White, J. B., Miadlikowska, J., Arnold, A. E., Miller, M. A., Magain, N., Uren, J. M., & Lutzoni, F. (2019). T-BAS Version 2.1: Tree-Based Alignment Selector toolkit for evolutionary placement of DNA sequences and viewing alignments and specimen metadata on curated and custom trees. Microbiology Resource Announcements. doi:10.1128/MRA.00328-19
• Dietzel, K., Valle, D., Fierer, N., U'Ren, J. M., & Barberan, A. (2019). Geographical Distribution of Fungal Plant Pathogens in Dust Across the United States. FRONTIERS IN ECOLOGY AND EVOLUTION, 7.
• Taylor, M. J., Mannan, R. W., U'Ren, J. M., Garber, N. P., Gallery, R. E., & Arnold, A. E. (2019). Age-related variation in the oral microbiome of urban Cooper's hawks (Accipiter cooperii). BMC MICROBIOLOGY, 19.
• U'Ren, J. M., Lutzoni, F., Miadlikowska, J., Zimmerman, N. B., Carbone, I., May, G., & Arnold, A. E. (2019). Host availability drives distributions of fungal endophytes in the imperilled boreal realm. NATURE ECOLOGY & EVOLUTION, 3(10), 1430-1437.
• Uren, J. M., Harrington, A., del Olmo-Ruiz, M., Garcia, K., Sandberg, D., Huang, Y., Hoffman, M. T., & Arnold, A. E. (2019). Coniochaeta endophytica sp. nov., a foliar endophyte associated with healthy photosynthetic tissue of Platycladus orientalis (Cupressaceae). Plant and Fungal Systematics, 64, 65–79. doi:10.2478/pfs-2019-0008
• Huang, Y., Bowman, E. A., Massimo, N., Garber, N. P., Uren, J. M., Sandberg, D. C., & Arnold, A. E. (2018). Using collections data to infer biogeographic, environmental, and host structure in communities of endophytic fungi. Mycologia. doi:doi: 10.1080/00275514.2018.1442078.
• Padumadasa, C., Xu, Y., Wijeratne, E. K., Espinosa-Artiles, P., Uren, J. M., Arnold, A. E., & Gunatilaka, L. (2018). Cytotoxic and Other Metabolites from Teratosphaeria sp. FL2137, a fungus associated with foliage of Pinus clausa. Journal of Natural Products. doi:10.1021/acs.jnatprod.7b00838
• Carbone, I., White, J. B., Miadlikowska, J., Arnold, A. E., Miller, M. A., Kauff, F., U'Ren, J. M., May, G., & Lutzoni, F. (2017). T-BAS: Tree-Based Alignment Selector toolkit for phylogenetic-based placement, alignment downloads and metadata visualization: an example with the Pezizomycotina tree of life. BIOINFORMATICS, 33(8), 1160-1168.
• Hurwitz, B. L., Ponsero, A., Thorton, Jr., J., & Uren, J. M. (2017). Phage hunters: Computational strategies for finding phages in large-scale 'omics datasets. Virus Research, Volume 244, 110-115. doi:https://doi.org/10.1016/j.virusres.2017.10.019
• Sarmiento, C., Zalamea, P., Dalling, J. W., Davis, A. S., Stump, S. M., U'Ren, J. M., & Arnold, A. E. (2017). Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 114(43), 11458-11463.
• Shaffer, J. P., U'Ren, J. M., Gallery, R. E., Baltrus, D. A., & Arnold, A. E. (2017). An Endohyphal Bacterium (Chitinophaga, Bacteroidetes) Alters Carbon Source Use by Fusarium keratoplasticum(F-solani Species Complex, Nectriaceae). FRONTIERS IN MICROBIOLOGY, 8.

Proceedings Publications

• Ponsero, A., Uren, J. M., Magain, N., Miadlikowska, J., Lutzoni, F., & Hurwitz, B. L. (2020, December). Metagenomic exploration of lichen thalli reveals novel viral communities. In American Geophysical Union Fall 2020.

Presentations

• Newton, A., Uren, J. M., Clark, M., Hunt, R., Nickerson, M., Commane, R., Baker, I. T., & Meredith, L. (2021). Understanding the Effect of Aboveground Vegetation Composition on Carbonyl Sulfide and Carbon Dioxide Fluxes in Alaskan Tundra and Boreal Biomes. AGU Fall Meeting 2021. New Orleans, LA: American Geophysical Union.
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  Extended daylight hours during the growing season in Alaska challenges traditional methods used to partition carbon dioxide (CO2) ecosystem fluxes into photosynthesis and respiration. Recently, carbonyl sulfide (OCS) has been investigated as an alternative to carbon dioxide as an independent atmospheric tracer for photosynthesis, but its dynamics have not been characterized in boreal and tundra biomes. Another barrier to making ecosystem-scale observations is vegetation heterogeneity, such that small scale field flux measurements may not be representative of the larger area. Our work will characterize the net OCS and CO2 fluxes in field and laboratory settings and ask how the vegetation composition affects these fluxes.Net OCS and CO2 fluxes from four sites in Alaska (Healy, Delta Junction, Poker Flats Research Range and Bonanza Creek) were measured in the field and again in a laboratory setting. In both cases, vegetation was left intact. Field fluxes were measured with a portable infra-red gas analyzer and dynamic acrylic flux chamber under light and dark conditions. Soil cores and vegetation were collected for laboratory analysis by a high precision infra-red gas analyzer using a dynamic flow through system to mimic field conditions. To isolate the drivers of these fluxes, soil cores were measured in three parts: whole, vegetation layer, and soil layer.Here we will present OCS and CO2 flux data from four Alaskan sites and discuss how differences in vegetation affects these fluxes. The information presented will add a crucial dataset that can be used for carbon cycle modeling and give insights into scaling up measurements from this heterogeneous landscape.
• Uren, J. M. (2021). Lichen mycobiota: evolutionary and ecological factors driving endolichenic fungal communities. 9th International Association for Lichenology Meeting. Virtual Conference: International Association for Lichenology.
• Uren, J. M. (2020, January). Phylogenetic Insights into the Endophyte Symbiosis using PacBio Ribosomal DNA Sequencing.. International Plant and Animal Genome Conference XXVIII. San Diego, CA.
• Uren, J. M. (2019, January). Microbial Communities in the Phyllosphere of B2-TRF. Biosphere 2 Tropical Rainforest WALD Research Workshop. Biosphere 2: University of Arizona.
• Uren, J. M. (2019, July). Circumglobal diversity and distributions of endophytic fungi in boreal plants and lichens.. Early Career Investigator Symposium, "Life at the Edge", Botanical Society of America Meeting. Tucson, AZ: International Association for Plant Taxonomy,.
• Uren, J. M. (2019, November). Linking phyllosphere fungal communities to functional traits. Northern Arizona University, Department of Biology, Fall Seminar Series. Flagstaff, AZ: Northern Arizona University.
• Uren, J. M., Nickerson, M., Moore, L. P., Endara, L., & Burleigh, J. G. (2019, August). Influence of host phylogeny and leaf chemistry on foliar endophytic communities of Quercus.. Mycological Society of America Annual Meeting. St. Paul, MN: Mycological Society of America.
• Uren, J. M. (2018, November). Linking phyllosphere fungal community assembly, evolutionary history, and metabolic diversity to ecosystem function. Ecosystem Genomics Seminar. BIO5.
• Uren, J. M. (2018, September). Linking Endophyte Community Assembly, Evolutionary History, and Functional Traits. Microbial Ecology and Evolution in the Phyllosphere. Santa Barbara, CA: Kavli Institute for Theoretical Physics, University of California Santa-Barbara.
• Uren, J. M., Carbone, I., & Arnold, A. E. (2018, July). Merging endophytes into the Xylariceae tree of life: insights gained from large-scale multilocus phylogenetic analyses. International Mycological Congress. San Juan, Puerto Rico.
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  Workshop at IMC on Xylariaceae

Poster Presentations

• Uren, J. M., Nickerson, M., Moore, L. P., Endara, L., & Burleigh, J. G. (2019, March). Influence of host phylogeny and leaf chemistry on foliar endophytic communities of Quercus.. 30th Fungal Genetics Meeting. Asilomar, CA: Genetics Society of America.
• Uren, J. M., Wisecaver, J., & Arnold, A. E. (2019, March). Comparative and population genomics of endophytic Xylariaceae. Department of Energy Joint Genome Institute Genomics of Energy and the Environment. San Francisco, CA: Department of Energy Joint Genome Institute.
• Arnold, A. E., Uren, J. M., Trouet, V. M., & Oita, S. (2018, August). Relationships of foliar endophyte communities in Picea mariana to tree age, biomass, and latitude. International Symbiosis Society.
• Barberan, A., Dietzel, K., Valle, D., & Uren, J. M. (2018, August). Understanding the geographical distribution of fungal plant pathogens. 17th International Symposium on Microbial Ecology. Leipzig, Germany.
• Young, J. C., Meredith, L., Sengupta, A., Van Haren, J. L., Uren, J. M., Uren, J. M., Sengupta, A., Van Haren, J. L., Young, J. C., & Meredith, L. (2017, Dec). Microbial drivers of spatial heterogeneity of nitrous oxide pulse dynamics following drought in an experimental tropical rainforest. AGU International Annual Meeting. New Orleans, LA.
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  Nitrous oxide (N2O) is a long-lived, potent greenhouse gas with increasing atmospheric concentrations. Soil microbes in agricultural and natural ecosystems are the dominant source of N2O, which involves complex interactions between N-cycling microbes, metabolisms, soil properties, and plants. Tropical rainforests are the largest natural source of N2O, however the microbial and environmental drivers are poorly understood as few studies have been performed in these environments. Thus, there is an urgent need for further research to fill in knowledge gaps regarding tropical N-cycling, and the response of soil microbial communities to changes in precipitation patterns, temperature, nitrogen deposition, and land use. To address this data gap, we performed a whole-forest drought in the tropical rainforest biome in Biosphere 2 (B2) and analyzed connections between soil microbes, forest heterogeneity, and N2O emissions. The B2 rainforest is the hottest tropical rainforest on Earth, and is an important model system for studying the response of tropical forests to warming with controlled experimentation. In this study, we measured microbial community abundance and diversity profiles (16S rRNA and ITS2 amplicon sequencing) along with their association with soil properties (e.g. pH, C, N) during the drought and rewetting at five locations (3 depths), including regions that have been previously characterized with high and low N2O drought pulse dynamics (van Haren et al., 2005). In this study, we present the spatial distribution of soil microbial communities within the rainforest at Biosphere 2 and their correlations with edaphic factors. In particular, we focus on microbial, soil, and plant factors that drive high and low N2O pulse zones. As in the past, we found that N2O emissions were highest in response to rewetting in a zone hypothesized to be rich in nutrients from a nearby sugar palm. We will characterize microbial indicator species and nitrogen cycling genes to better resolve N cycling across the forest. Understanding how N2O formation is mediated by soil microbes in response to drought in tropical rainforests is challenging given the great diversity of microbial communities and metabolisms involved, but is critical for understanding the source of global increases in atmospheric N2O.