Environmental drivers and cryptic biodiversity hotspots define endophytes in Earth's largest terrestrial biome.

Understanding how symbiotic associations differ across environmental gradients is key to predicting the fate of symbioses as environments change, and it is vital for detecting global reservoirs of symbiont biodiversity in a changing world.1,2,3 However, sampling of symbiotic partners at the full-biome scale is difficult and rare. As Earth's largest terrestrial biome, boreal forests influence carbon dynamics and climate regulation at a planetary scale. Plants and lichens in this biome host the highest known phylogenetic diversity of fungal endophytes, which occur within healthy photosynthetic tissues and can influence hosts' resilience to stress.4,5 We examined how communities of endophytes are structured across the climate gradient of the boreal biome, focusing on the dominant plant and lichen species occurring across the entire south-to-north span of the boreal zone in eastern North America. Although often invoked for understanding the distribution of biodiversity, neither a latitudinal gradient nor mid-domain effect5,6,7 can explain variation in endophyte diversity at this trans-biome scale. Instead, analyses considering shifts in forest characteristics, Picea biomass and age, and nutrients in host tissues from 46° to 58° N reveal strong and distinctive signatures of climate in defining endophyte assemblages in each host lineage. Host breadth of endophytes varies with climate factors, and biodiversity hotspots can be identified at plant-community transitions across the boreal zone at a global scale. Placed against a backdrop of global circumboreal sampling,4 our study reveals the sensitivity of endophytic fungi, their reservoirs of biodiversity, and their important symbiotic associations, to climate.

Communities of endophytic fungi in a Puerto Rican rainforest vary along a gradient of disturbance due to Hurricane Maria.

Increases in the frequency and intensity of hurricanes influence the structure, function, and resilience of Caribbean forests. Trees in such forests harbor diverse fungal endophytes within leaves and roots. Fungal endophytes often are important for plant health and stress responses, but how their communities are impacted by hurricanes is not well known. We measured forest disturbance in Carite State Forest in Puerto Rico ca. 16 months after the passage of Hurricane Maria, a Category 4 storm. In three sites, each comprising three plots representing a local gradient of hurricane disturbance, we evaluated soil chemistry and used culture-free analyses to measure richness, phylogenetic diversity, and composition of endophyte communities in leaves and roots. We found that endophyte richness did not vary significantly among plant families or as a function of soil chemistry. Instead, leaf endophytes peaked in richness and decreased in phylogenetic diversity at intermediate levels of disturbance. Root endophytes did not show such variation, but both leaf- and root endophyte communities differed in species composition as a function of disturbance across the forest. Locations with less disturbance typically hosted distinctive assemblages of foliar endophytes, whereas more disturbed locations had more regionally homogeneous endophyte communities. Together, our results show that changes in endophyte richness and phylogenetic diversity can be detected in aboveground tissues more than a year after major storms. In turn, pervasive shifts in endophyte community composition both aboveground and belowground suggest a subtle and lasting effect of hurricanes that merits further study, potentially contributing to the promotion of spatially heterogeneous endophyte assemblages at a landscape scale in these diverse island forests.

Los aumentos en la frecuencia e intensidad de los huracanes influyen en la estructura, función, y resiliencia de los bosques del Caribe. Los árboles en dichos bosques tienen diversos hongos endófitos dentro de las hojas y raíces. Los hongos endófitos pueden ser importantes para la salud de las plantas y las respuestas a el estrés, pero no se conoce bien cómo los huracanes afectan a sus comunidades. Medimos la perturbación forestal en el Bosque Estatal de Carite en Puerto Rico a 16 meses después del paso del Huracán María (huracán categoría 4). En tres sitios, cada uno de los cuales incluyeron tres parcelas que representan un gradiente local de perturbación debido al huracán, evaluamos la química del suelo y utilizamos análisis libres de cultivos para medir la riqueza, la diversidad filogenética y la composición de las comunidades de endófitos en las hojas y raíces de las plantas. Encontramos que la riqueza de endófitos no varió significativamente entre las familias de plantas o en función de la química del suelo. Los endófitos de hojas alcanzaron su punto máximo en riqueza y disminuyeron en diversidad filogenética en niveles intermedios de perturbación forestal. Los endófitos de raíces no mostraron tal variación, pero ambas comunidades de endófitos difirieron en la composición de especies en función de la perturbación en el bosque. Las ubicaciones con menos perturbaciones generalmente tenían conjuntos distintivos de endófitos foliares, mientras que las ubicaciones más perturbadas tenían comunidades de endófitos regionalmente más homogéneas. Nuestros resultados muestran que los cambios en la riqueza de endófitos y la diversidad filogenética se pueden detectar en los tejidos de las hojas más de un año después de grandes tormentas. A su vez, los cambios generalizados en la composición de la comunidad de endófitos de hojas y raíces sugieren un efecto sutil y duradero de los huracanes que amerita un mayor estudio, lo que podría contribuir a la promoción de ensamblajes de comunidades de endófitos heterogéneas en diversos bosques.

Mycology: Metagenomes illuminate evolutionary relationships and reframe symbiotic interactions.

An intriguing new study leverages newly generated metagenomes to remap the evolution of the most species-rich clade of fungi, highlighting how some of the most intriguing and visible manifestations of symbioses - lichens - may arise.

Wild microbiomes of striped plateau lizards vary with reproductive season, sex, and body size.

Long-term studies of animal microbiomes under natural conditions are valuable for understanding the effects of host demographics and environmental factors on host-associated microbial communities, and how those effects interact and shift over time. We examined how the cloacal microbiome of wild Sceloporus virgatus (the striped plateau lizard) varies under natural conditions in a multi-year study. Cloacal swabs were collected from wild-caught lizards across their entire active season and over three years in southeastern Arizona, USA. Analyses of 16S rRNA data generated on the Illumina platform revealed that cloacal microbiomes of S. virgatus vary as a function of season, sex, body size, and reproductive state, and do so independently of one another. Briefly, microbial diversity was lowest in both sexes during the reproductive season, was higher in females than in males, and was lowest in females when they were vitellogenic, and microbiome composition varied across seasons, sexes, and sizes. The pattern of decreased diversity during reproductive periods with increased sociality is surprising, as studies in other systems often suggest that microbial diversity generally increases with sociality. The cloacal microbiome was not affected significantly by hibernation and was relatively stable from year to year. This study highlights the importance of long term, wide-scale microbiome studies for capturing accurate perspectives on microbiome diversity and composition in animals. It also serves as a warning for comparisons of microbiomes across species, as each may be under a different suite of selective pressures or exhibit short-term variation from external or innate factors, which may differ in a species-specific manner.

Acrogenospora terricola sp. nov., a fungal species associated with seeds of pioneer trees in the soil seed bank of a lowland forest in Panama.

As currently circumscribed, Acrogenospora (Acrogenosporaceae, Minutisphaerales, Dothideomycetes) is a genus of saprobic hyphomycetes with distinctive conidia. Although considered common and cosmopolitan, the genus is poorly represented by sequence data, and no neotropical representatives are present in public sequence databases. Consequently, Acrogenospora has been largely invisible to ecological studies that rely on sequence-based identification. As part of an effort to identify fungi collected during ecological studies, we identified strains of Acrogenospora isolated in culture from seeds in the soil seed bank of a lowland tropical forest in Panama. Here we describe Acrogenospora terricola sp. nov. based on morphological and phylogenetic analyses. We confirm that the genus has a pantropical distribution. The observation of Acrogenospora infecting seeds in a terrestrial environment contrasts with previously described species in the genus, most of which occur on decaying wood in freshwater environments. This work highlights the often hidden taxonomic value of collections derived from ecological studies of fungal communities and the ways in which rich sequence databases can shed light on the identity, distributions and diversity of cryptic microfungi.

Traits along the leaf economics spectrum are associated with communities of foliar endophytic symbionts.

Leaf traits of plants worldwide are classified according to the Leaf Economics Spectrum (LES), which links leaf functional traits to evolutionary life history strategies. As a continuum ranging from thicker, tough leaves that are low in nitrogen (N) to thinner, softer, leaves that are high in N, the LES brings together physical, chemical, and ecological traits. Fungal endophytes are common foliar symbionts that occur in healthy, living leaves, especially in tropical forests. Their community composition often differs among co-occurring host species in ways that cannot be explained by environmental conditions or host phylogenetic relationships. Here, we tested the over-arching hypothesis that LES traits act as habitat filters that shape communities of endophytes both in terms of composition, and in terms of selecting for endophytes with particular suites of functional traits. We used culture-based and culture-free surveys to characterize foliar endophytes in mature leaves of 30 phylogenetically diverse plant species with divergent LES traits in lowland Panama, and then measured functional traits of dominant endophyte taxa in vitro. Endophytes were less abundant and less diverse in thick, tough, leaves compared to thin, softer, leaves in the same forest, even in closely related plants. Endophyte communities differed according to leaf traits, including leaf punch strength and carbon and nitrogen content. The most common endophyte taxa in leaves at different ends of the LES differ in their cellulase, protease, chitinase, and antipathogen activity. Our results extend the LES framework for the first time to diverse and ecologically important endophytes, opening new hypotheses regarding the degree to which foliar symbionts respond to, and extend, the functional traits of leaves they inhabit.

Bacterial-fungal interactions: Bacteria take up residence in the house that Fungi built.

Interactions between bacteria and fungi are widespread in nature. New work shows that bacteria not known to have an endofungal lifestyle can take advantage of environmentally resistant fungal structures that are induced by lipopeptides from other bacteria. Diverse bacterial communities can flourish in these refugia to survive stressful conditions.

Transcriptional Profiles of a Foliar Fungal Endophyte (Pestalotiopsis, Ascomycota) and Its Bacterial Symbiont (Luteibacter, Gammaproteobacteria) Reveal Sulfur Exchange and Growth Regulation during Early Phases of Symbiotic Interaction.

Symbiosis with bacteria is widespread among eukaryotes, including fungi. Bacteria that live within fungal mycelia (endohyphal bacteria) occur in many plant-associated fungi, including diverse Mucoromycota and Dikarya. Pestalotiopsis sp. strain 9143 is a filamentous ascomycete isolated originally as a foliar endophyte of Platycladus orientalis (Cupressaceae). It is infected naturally with the endohyphal bacterium Luteibacter sp. strain 9143, which influences auxin and enzyme production by its fungal host. Previous studies have used transcriptomics to examine similar symbioses between endohyphal bacteria and root-associated fungi such as arbuscular mycorrhizal fungi and plant pathogens. However, currently there are no gene expression studies of endohyphal bacteria of Ascomycota, the most species-rich fungal phylum. To begin to understand such symbioses, we developed methods for assessing gene expression by Pestalotiopsis sp. and Luteibacter sp. when grown in coculture and when each was grown axenically. Our assays showed that the density of Luteibacter sp. in coculture was greater than in axenic culture, but the opposite was true for Pestalotiopsis sp. Dual-transcriptome sequencing (RNA-seq) data demonstrate that growing in coculture modulates developmental and metabolic processes in both the fungus and bacterium, potentially through changes in the balance of organic sulfur via methionine acquisition. Our analyses also suggest an unexpected, potential role of the bacterial type VI secretion system in symbiosis establishment, expanding current understanding of the scope and dynamics of fungal-bacterial symbioses. IMPORTANCE Interactions between microbes and their hosts have important outcomes for host and environmental health. Foliar fungal endophytes that infect healthy plants can harbor facultative endosymbionts called endohyphal bacteria, which can influence the outcome of plant-fungus interactions. These bacterial-fungal interactions can be influential but are poorly understood, particularly from a transcriptome perspective. Here, we report on a comparative, dual-RNA-seq study examining the gene expression patterns of a foliar fungal endophyte and a facultative endohyphal bacterium when cultured together versus separately. Our findings support a role for the fungus in providing organic sulfur to the bacterium, potentially through methionine acquisition, and the potential involvement of a bacterial type VI secretion system in symbiosis establishment. This work adds to the growing body of literature characterizing endohyphal bacterial-fungal interactions, with a focus on a model facultative bacterial-fungal symbiosis in two species-rich lineages, the Ascomycota and Proteobacteria.

Comparative transcriptomics of fungal endophytes in co-culture with their moss host Dicranum scoparium reveals fungal trophic lability and moss unchanged to slightly increased growth rates.

Mosses harbor fungi whose interactions within their hosts remain largely unexplored. Trophic ranges of fungal endophytes from the moss Dicranum scoparium were hypothesized to encompass saprotrophism. This moss is an ideal host to study fungal trophic lability because of its natural senescence gradient, and because it can be grown axenically. Dicranum scoparium was co-cultured with each of eight endophytic fungi isolated from naturally occurring D. scoparium. Moss growth rates, and gene expression levels (RNA sequencing) of fungi and D. scoparium, were compared between axenic and co-culture treatments. Functional lability of two fungal endophytes was tested by comparing their RNA expression levels when colonizing living vs dead gametophytes. Growth rates of D. scoparium were unchanged, or increased, when in co-culture. One fungal isolate (Hyaloscyphaceae sp.) that promoted moss growth was associated with differential expression of auxin-related genes. When grown with living vs dead gametophytes, Coniochaeta sp. switched from having upregulated carbohydrate transporter activity to upregulated oxidation-based degradation, suggesting an endophytism to saprotrophism transition. However, no such transition was detected for Hyaloscyphaceae sp. Individually, fungal endophytes did not negatively impact growth rates of D. scoparium. Our results support the long-standing hypothesis that some fungal endophytes can switch to saprotrophism.

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. Overall, 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.

Coniochaeta elegans sp. nov., Coniochaeta montana sp. nov. and Coniochaeta nivea sp. nov., three new species of endophytes with distinctive morphology and functional traits.

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 Coniochaeta (Sacc.) Cooke (Coniochaetaceae, Coniochaetales, Sordariomycetes, Ascomycota) are commonly isolated on standard media, but rarely are characterized. We examined 26 isolates of Coniochaeta 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 Coniochaeta cymbiformispora, 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: Coniochaeta elegans sp. nov., Coniochaeta montana sp. nov. and Coniochaeta nivea sp. nov. Each has a wide host range, including lichens, bryophytes and vascular plants. C. elegans sp. nov. and C. nivea sp. nov. have wide geographic ranges. C. montana 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 in vitro. Overall, this study provides insight into the ecological and evolutionary diversity of Coniochaeta and suggests that these strains may be amenable for studies of traits relevant to a horizontally transmitted, symbiotic lifestyle.

Strobiloscyphones A-F, 6-Isopentylsphaeropsidones and Other Metabolites from Strobiloscypha sp. AZ0266, a Leaf-Associated Fungus of Douglas Fir.

Six new 6-isopentylsphaeropsidones, strobiloscyphones A-F (1-6), and a new hexadecanoic acid, (2Z,4E,6E)-8,9-dihydroxy-10-oxohexadeca-2,4,6-trienoic acid (7), together with sphaeropsidone (8) and its known synthetic analogue 5-dehydrosphaeropsidone (9) were isolated from Strobiloscypha sp. AZ0266, a fungus inhabiting the leaf litter of Douglas fir (Pseudotsuga menziesii). The structures of 1-7 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 (6) contains a novel highly oxygenated tetracyclic oxireno-octahydrodibenzofuran ring system. Natural products 1, 6, and 9 and the semisynthetic analogue 12 derived from 8 exhibited cytotoxic activity, whereas 9 and 12 showed antimicrobial activity. Possible biosynthetic pathways to 1-6, 8, and 9 are proposed.

Drivers and implications of distance decay differ for ectomycorrhizal and foliar endophytic fungi across an anciently fragmented landscape.

Fungal communities associated with plants often decrease in similarity as the distance between sampling sites increases (i.e., they demonstrate distance decay). In the southwestern USA, forests occur in highlands separated from one another by warmer, drier biomes with plant and fungal communities that differ from those at higher elevations. These disjunct forests are broadly similar in climate to one another, offering an opportunity to examine drivers of distance decay in plant-associated fungi across multiple ecologically similar yet geographically disparate landscapes. We examined ectomycorrhizal and foliar endophytic fungi associated with a dominant forest tree (Pinus ponderosa) in forests across ca. 550 km of geographic distance from northwestern to southeastern Arizona (USA). Both guilds of fungi showed distance decay, but drivers differed for each: ectomycorrhizal fungi are constrained primarily by dispersal limitation, whereas foliar endophytes are constrained by specific environmental conditions. Most ectomycorrhizal fungi were found in only a single forested area, as were many endophytic fungi. Such regional-scale perspectives are needed for baseline estimates of fungal diversity associated with forest trees at a landscape scale, with attention to the sensitivity of different guilds of fungal symbionts to decreasing areas of suitable habitat, increasing disturbance, and related impacts of climate change.

Climate and seasonality drive the richness and composition of tropical fungal endophytes at a landscape scale.

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.

Methodological Approaches Frame Insights into Endophyte Richness and Community Composition.

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.

Teratopyrones A-C, Dimeric Naphtho-γ-Pyrones and Other Metabolites from Teratosphaeria sp. AK1128, a Fungal Endophyte of Equisetum arvense.

Bioassay-guided fractionation of a cytotoxic extract derived from a solid potato dextrose agar (PDA) culture of Teratosphaeria sp. AK1128, a fungal endophyte of Equisetum arvense, afforded three new naphtho-γ-pyrone dimers, teratopyrones A-C (1-3), together with five known naphtho-γ-pyrones, aurasperone B (4), aurasperone C (5), aurasperone F (6), nigerasperone A (7), and fonsecin B (8), and two known diketopiperazines, asperazine (9) and isorugulosuvine (10). The structures of 1-3 were determined on the basis of their spectroscopic data. Cytotoxicity assay revealed that nigerasperone A (7) 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 IC50s ranging from 2.37 to 4.12 µM while other metabolites exhibited no cytotoxic activity up to a concentration of 5.0 µM.

An epigenetic modifier induces production of 3-(4-oxopyrano)-chromen-2-ones in Aspergillus sp. AST0006, an endophytic fungus of Astragalus lentiginosus.

Incorporation of the epigenetic modifier suberoylanilide hydroxamic acid (SAHA) into a potato dextrose broth culture of the endophytic fungus Aspergillus sp. AST0006 affected its polyketide biosynthetic pathway providing two new 3-(4-oxopyrano)-chromen-2-ones, aspyranochromenones A (1) and B (2), and the isocoumarin, (-)-6,7-dihydroxymellein (3). Eight additional metabolites (4-11) and two biotransformation products of SAHA (12-13) were also encountered. The planar structures and relative configurations of the new metabolites 1-2 were elucidated with the help of high-resolution mass, 1D and 2D NMR spectroscopic data and the absolute configurations of 1-3 were determined by comparison of experimental and calculated ECD data. Possible biosynthetic pathways to 1 and 2 are presented.

Diversity and distribution of microbial communities in floral nectar of two night-blooming plants of the Sonoran Desert.

Nectar-inhabiting microbes are increasingly appreciated as important components of plant-pollinator interactions. We quantified the incidence, abundance, diversity, and composition of bacterial and fungal communities in floral nectar of two night-blooming plants of the Sonoran Desert over the course of a flowering season: Datura wrightii (Solanaceae), which is pollinated by hawkmoths, and Agave palmeri (Agavaceae), which is pollinated by bats but visited by hawkmoths that forage for nectar. We examined the relevance of growing environment (greenhouse vs. field), time (before and after anthesis), season (from early to late in the flowering season), and flower visitors (excluded via mesh sleeves or allowed to visit flowers naturally) in shaping microbial assemblages in nectar. We isolated and identified bacteria and fungi from >300 nectar samples to estimate richness and taxonomic composition. Our results show that microbes were common in D. wrightii and A. palmeri nectar in the greenhouse but more so in field environments, both before and especially after anthesis. Bacteria were isolated more frequently than fungi. The abundance of microbes in nectar of D. wrightii peaked near the middle of the flowering season. Microbes generally were more abundant as time for floral visitation increased. The composition of bacterial and especially fungal communities differed significantly between nectars of D. wrightii and A. palmeri, opening the door to future studies examining their functional roles in shaping nectar chemistry, attractiveness, and pollinator specialization.

Host availability drives distributions of fungal endophytes in the imperilled boreal realm.

Boreal forests represent the world's largest terrestrial biome and provide ecosystem services of global importance. Highly imperilled by climate change, these forests host Earth's greatest phylogenetic diversity of endophytes, a hyperdiverse group of symbionts that are defined by their occurrence within living, symptomless plant and lichen tissues. Endophytes shape the ecological and evolutionary trajectories of plants and are therefore key to the function and resilience of terrestrial ecosystems. A critical step in linking the ecological functions of endophytes with those of their hosts is to understand the distributions of these symbionts at the global scale; however, turnover in host taxa with geography and climate can confound insights into endophyte biogeography. As a result, global drivers of endophyte diversity and distributions are not known. Here, we leverage sampling from phylogenetically diverse boreal plants and lichens across North America and Eurasia to show that host filtering in distinctive environments, rather than turnover with geographical or environmental distance, is the main determinant of the community composition and diversity of endophytes. We reveal the distinctiveness of boreal endophytes relative to soil fungi worldwide and endophytes from diverse temperate biomes, highlighting a high degree of global endemism. Overall, the distributions of endophytes are directly linked to the availability of compatible hosts, highlighting the role of biotic interactions in shaping fungal communities across large spatial scales, and the threat that climate change poses to biological diversity and function in the imperilled boreal realm.