Cytological studies reveal high variation in ascospore number and shape and conidia produced directly from ascospores in Morchella galilaea.

Spores are important as dispersal and survival propagules in fungi. In this study we investigated the variation in number, shape, size and germination mode of ascospores in Morchella galilaea, the only species of the genus Morchella known to fruit in the autumn. Based on the observation of five samples, we first discovered significant variation in the shape and size of ascospores in Morchella. One to sixteen ascospores were found in the asci. Ascospore size correlated negatively with ascospore number, but positively with ascus size, and ascus size was positively correlated with ascospore number. We noted that ascospores, both from fresh collections and dried specimens, germinated terminally or laterally either by extended germ tubes, or via the production of conidia that were formed directly from ascospores at one, two or multiple sites. The direct formation of conidia from ascospores takes place within asci or after ascospores are discharged. Using laser confocal microscopy, we recorded the number of nuclei in ascospores and in conidia produced from ascospores. In most ascospores of M. galilaea, several nuclei were observed, as is typical of species of Morchella. However, nuclear number varied from zero to around 20 in this species, and larger ascospores harbored more nuclei. One to six nuclei were present in the conidia. Nuclear migration from ascospores to conidia was observed. Conidia forming directly from ascospores has been observed in few species of Pezizomycetes; this is the first report of the phenomenon in Morchella species. Morphological and molecular data show that conidial formation from ascospores is not found in all the specimens of this species and, hence, is not an informative taxonomic character in M. galilaea. Our data suggest that conidia produced from ascospores and successive mitosis within the ascus may contribute to asci with more than eight spores. The absence of mitosis and/or nuclear degeneration, as well as cytokinesis defect, likely results in asci with fewer than eight ascospores. This study provides new insights into the poorly understood life cycle of Morchella species and more broadly improves knowledge of conidia formation and reproductive strategies in Pezizomycetes.

A new species of Inosperma, and first record of I. afromelliolens (Inocybaceae, Fungi) from West Africa.

Here, we present the newly identified Inosperma macrocarpa and the first record of I. afromelliolens from West Africa. Inosperma macrocarpa is nested in an Old World Tropical clade, based on a molecular phylogeny inferred from the sequences of ITS, LSU, RPB2, and TEF1. Complete descriptions and illustrations, including photographs and line drawings, of the new species are presented. Morphological and molecular analyses based on collections from Benin confirmed the presence of I. afromelliolens in West Africa. Toxicity analysis showed that neither species contained muscarine, which further supports the hypothesis that the ability to produce muscarine is a derived trait of Inosperma.

How, not if, is the question mycologists should be asking about DNA-based typification.

Fungal metabarcoding of substrates such as soil, wood, and water is uncovering an unprecedented number of fungal species that do not seem to produce tangible morphological structures and that defy our best attempts at cultivation, thus falling outside the scope of the International Code of Nomenclature for algae, fungi, and plants. The present study uses the new, ninth release of the species hypotheses of the UNITE database to show that species discovery through environmental sequencing vastly outpaces traditional, Sanger sequencing-based efforts in a strongly increasing trend over the last five years. Our findings challenge the present stance of some in the mycological community - that the current situation is satisfactory and that no change is needed to "the code" - and suggest that we should be discussing not whether to allow DNA-based descriptions (typifications) of species and by extension higher ranks of fungi, but what the precise requirements for such DNA-based typifications should be. We submit a tentative list of such criteria for further discussion. The present authors hope for a revitalized and deepened discussion on DNA-based typification, because to us it seems harmful and counter-productive to intentionally deny the overwhelming majority of extant fungi a formal standing under the International Code of Nomenclature for algae, fungi, and plants.

Historical biogeography and diversification of ringless Amanita (section Vaginatae) support an African origin and suggest niche conservatism in the Americas.

Ectomycorrhizal fungi (ECM) sustain nutrient recycling in most terrestrial ecosystems, yet we know little about what major biogeographical events gave rise to present-day diversity and distribution patterns. Given the strict relationship between some ECM lineages and their hosts, geographically well-sampled phylogenies are central to understanding major evolutionary processes of fungal biodiversity patterns. Here, we focus on Amanita sect. Vaginatae to address global diversity and distribution patterns. Ancestral-state-reconstruction based on a 4-gene timetree with over 200 species supports an African origin between the late Paleocene and the early Eocene (ca. 56 Ma). Major biogeographic "out-of-Africa" events include multiple dispersal events to Southeast Asia (ca. 45-21 Ma), Madagascar (ca. 18 Ma), and the current Amazonian basin (ca. 45-36 Ma), the last two likely trans-oceanic. Later events originating in Southeast Asia involve Nearctic dispersal to North America (ca. 20-5 Ma), Oceania (Australia and New Zealand; ca. 15 Ma), and Europe (ca. 10-5 Ma). Subsequent dispersals were also inferred from Southeast Asia to East Asia (ca. 4 Ma); from North America to East Asia (ca. 11-8 Ma), Southeast Asia (ca. 19-2 Ma), Northern Andes (ca. 15 Ma), and Europe (ca. 15-2 Ma), respectively; and from the Amazon to the Caribbean region (ca. 25-20 Ma). Finally, we detected a significant increase in the net diversification rates in the branch leading to most northern temperate species in addition to higher state-dependent diversification rates in temperate lineages, consistent with previous findings. These results suggest that species of sect. Vaginatae likely have higher dispersal ability and higher adaptability to new environments, in particular compared to those of its sister clade, sect. Caesareae. Overall, the much wider distribution of A. sect. Vaginatae, from pan-tropical to pan-arctic, provides a unique window to understanding niche conservatism across a species-rich clade of ECM fungi.

Impact of model assumptions on the inference of the evolution of ectomycorrhizal symbiosis in fungi.

Ectomycorrhiza (ECM) is a symbiotic relation between plant and fungi that is essential for nutrient uptake of many stand forming trees. There are two conflicting views about the evolution of ECM in fungi suggesting (1) relatively few transitions to ECM followed by reversals to non-ECM, or (2) many independent origins of ECM and no reversals. In this study, we compare these, and other, hypotheses and test the impact of different models on inference. We assembled a dataset of five marker gene sequences (nuc58, nucLSU, nucSSU, rpb1, and rpb2) and 2,174 fungal taxa covering the three subphyla: Agaricomycotina, Mucoromycotina and Pezizomycotina. The fit of different models, including models with variable rates in clades or through time, to the pattern of ECM fungal taxa was tested in a Bayesian framework, and using AIC and simulations. We find that models implementing variable rates are a better fit than models without rate shift, and that the conclusion about the relative rate between ECM and non-ECM depend largely on whether rate shifts are allowed or not. We conclude that standard constant-rate ancestral state reconstruction models are not adequate for the analysis of the evolution of ECM fungi, and may give contradictory results to more extensive analyses.

Stage-specific transposon activity in the life cycle of the fairy-ring mushroom Marasmius oreades.

Genetic variability can be generated by different mechanisms, and across the life cycle. Many basidiomycete fungi have an extended somatic stage, during which each cell carries two genetically distinct haploid nuclei (dikaryosis), resulting from fusion of two compatible monokaryotic individuals. Recent findings have revealed remarkable genome stability at the nucleotide level during dikaryotic growth in these organisms, but whether this pattern extends to mutations affecting large genomic regions remains unknown. Furthermore, despite high genome integrity during dikaryosis, basidiomycete populations are not devoid of genetic diversity, begging the question of when this diversity is introduced. Here, we used a Marasmius oreades fairy ring to investigate the rise of large-scale variants during mono- and dikaryosis. By separating the two nuclear genotypes from four fruiting bodies and generating complete genome assemblies, we gained access to investigate genomic changes of any size. We found that during dikaryotic growth in nature the genome stayed intact, but after separating the nucleotypes into monokaryons, a considerable amount of structural variation started to accumulate, driven to large extent by transposons. Transposon insertions were also found in monokaryotic single-meiospore isolates. Hence, we show that genome integrity in basidiomycetes can be interrupted during monokaryosis, leading to genomic rearrangements and increased activity of transposable elements. We suggest that genetic diversification is disproportionate between life cycle stages in mushroom-forming fungi, so that the short-lived monokaryotic growth stage is more prone to genetic changes than the dikaryotic stage.

Phylogeny and evolution of morphological structures in a highly diverse lineage of fruiting-body-forming amoebae, order Trichiales (Myxomycetes, Amoebozoa).

Early phylogenetic studies refuted most previous assumptions concerning the evolution of the morphological traits in the fruiting bodies of the order Trichiales and did not detect discernible evolutionary patterns, yet they were based on a limited number of species. We infer a new Trichiales phylogeny based on three independently inherited genetic regions (nuclear and mitochondrial), with a fair taxonomic sampling encompassing its broad diversity. Besides, we study the evolutionary history of some key morphological characters. According to the new phylogeny, most fruiting body traits in Trichiales systematics do not represent exclusive synapomorphies or autapomorphies for most monophyletic groups. Instead, the evolution of the features derived from the peridium, stalk, capillitium, and spores showed intricate patterns, and character state transitions occurred rather within- than between clades. Thus, we should consider other evolutionary scenarios instead of assuming the homology of some characters. According to these results, we propose a new classification of Trichiales, including the creation of a new genus, Gulielmina, the resurrection of the family Dictydiaethaliaceae and the genus Ophiotheca, and the proposal of 13 new combinations for species of the genera Arcyria (1), Hemitrichia (2), Ophiotheca (2), Oligonema (4), Gulielmina (3), and Perichaena (1).

The curse of the uncultured fungus.

The international DNA sequence databases abound in fungal sequences not annotated beyond the kingdom level, typically bearing names such as "uncultured fungus". These sequences beget low-resolution mycological results and invite further deposition of similarly poorly annotated entries. What do these sequences represent? This study uses a 767,918-sequence corpus of public full-length fungal ITS sequences to estimate what proportion of the 95,055 "uncultured fungus" sequences that represent truly unidentifiable fungal taxa - and what proportion of them that would have been straightforward to annotate to some more meaningful taxonomic level at the time of sequence deposition. Our results suggest that more than 70% of these sequences would have been trivial to identify to at least the order/family level at the time of sequence deposition, hinting that factors other than poor availability of relevant reference sequences explain the low-resolution names. We speculate that researchers' perceived lack of time and lack of insight into the ramifications of this problem are the main explanations for the low-resolution names. We were surprised to find that more than a fifth of these sequences seem to have been deposited by mycologists rather than researchers unfamiliar with the consequences of poorly annotated fungal sequences in molecular repositories. The proportion of these needlessly poorly annotated sequences does not decline over time, suggesting that this problem must not be left unchecked.

Soil fungal communities of ectomycorrhizal dominated woodlands across West Africa.

Forests and woodlands in the West African Guineo-Sudanian transition zone contain many tree species that form symbiotic interactions with ectomycorrhizal (ECM) fungi. These fungi facilitate plant growth by increasing nutrient and water uptake and include many fruiting body-forming fungi, including some edible mushrooms. Despite their importance for ecosystem functioning and anthropogenic use, diversity and distribution of ECM fungi is severely under-documented in West Africa. We conducted a broad regional sampling across five West African countries using soil eDNA to characterize the ECM as well as the total soil fungal community in gallery forests and savanna woodlands dominated by ECM host tree species. We subsequently sequenced the entire ITS region and much of the LSU region to infer a phylogeny for all detected soil fungal species. Utilizing a long read sequencing approach allows for higher taxonomic resolution by using the full ITS region, while the highly conserved LSU gene allows for a more accurate higher-level assignment of species hypotheses, including species without ITS-based taxonomy assignments. We detect no overall difference in species richness between gallery forests and woodlands. However, additional gallery forest plots and more samples per plot would have been needed to firmly conclude this pattern. Based on both abundance and richness, species from the families Russulaceae and Inocybaceae dominate the ECM fungal soil communities across both vegetation types. The community structure of both total soil fungi and ECM fungi was significantly influenced by vegetation types and showed strong correlation within plots. However, we found no significant difference in fungal community structure between samples collected adjacent to different host tree species within each plot. We conclude that within plots, the fungal community is structured more by the overall ECM host plant community than by the species of the individual host tree that each sample was collected from.

Long- and short-read metabarcoding technologies reveal similar spatiotemporal structures in fungal communities.

Fungi form diverse communities and play essential roles in many terrestrial ecosystems, yet there are methodological challenges in taxonomic and phylogenetic placement of fungi from environmental sequences. To address such challenges, we investigated spatiotemporal structure of a fungal community using soil metabarcoding with four different sequencing strategies: short-amplicon sequencing of the ITS2 region (300-400 bp) with Illumina MiSeq, Ion Torrent Ion S5 and PacBio RS II, all from the same PCR library, as well as long-amplicon sequencing of the full ITS and partial LSU regions (1200-1600 bp) with PacBio RS II. Resulting community structure and diversity depended more on statistical method than sequencing technology. The use of long-amplicon sequencing enables construction of a phylogenetic tree from metabarcoding reads, which facilitates taxonomic identification of sequences. However, long reads present issues for denoising algorithms in diverse communities. We present a solution that splits the reads into shorter homologous regions prior to denoising, and then reconstructs the full denoised reads. In the choice between short and long amplicons, we suggest a hybrid approach using short amplicons for sampling breadth and depth, and long amplicons to characterize the local species pool for improved identification and phylogenetic analyses.

Three new species of Inosperma (Agaricales, Inocybaceae) from Tropical Africa.

Here, we describe three new species of Inosperma from Tropical Africa: Inosperma africanum, I. bulbomarginatum and I. flavobrunneum. Morphological and molecular data show that these species have not been described before, hence need to be described as new. The phylogenetic placements of these species were inferred, based on molecular evidence from sequences of 28S and RPB2. Additional analysis using ITS dataset shows interspecific variation between each species. Phylogenetic analyses resolve I. flavobrunneum in Old World Tropical clade 1 with weak support, I. bulbomarginatum is sister of Old World Tropical clade 1 and I. africanum is indicated as sister to the rest of Inosperma. Complete description and illustrations, including photographs and line drawings, are presented for each species. A new combination of Inocybe shawarensis into Inosperma is also proposed.

Multigene phylogeny and taxonomic revision of Atheliales s.l.: Reinstatement of three families and one new family, Lobuliciaceae fam. nov.

Atheliales (Agaricomycetes, Basidiomycota) is an order mostly composed of corticioid fungi, containing roughly 100 described species in 20 genera. Members exhibit remarkable ecological diversity, including saprotrophs, ectomycorrhizal symbionts, facultative parasites of plants or lichens, and symbionts of termites. Ectomycorrhizal members are well known because they often form a major part of boreal and temperate fungal communities. However, Atheliales is generally understudied, and molecular data are scarce. Furthermore, the order is riddled with many taxonomic problems; some genera are non-monophyletic and several species have been shown to be more closely related to other orders. We investigated the phylogenetic position of genera that are currently listed in Atheliales sensu lato by employing an Agaricomycetes-wide dataset with emphasis on Atheliales including the type species of genera therein. A phylogenetic analysis based on 5.8S, LSU, rpb2, and tef1 (excluding third codon) retrieved Atheliales in subclass Agaricomycetidae, as sister to Lepidostromatales. In addition, a number of Atheliales genera were retrieved in other orders with strong support: Byssoporia in Russulales, Digitatispora in Agaricales, Hypochnella in Polyporales, Lyoathelia in Hymenochaetales, and Pteridomyces in Trechisporales. Based on this result, we assembled another dataset focusing on the clade with Atheliales sensu stricto and representatives from Lepidostromatales and Boletales as outgroups, based on ITS (ITS1-5.8S-ITS2), LSU, rpb2, and tef1. The reconstructed phylogeny of Atheliales returned five distinct lineages, which we propose here as families. Lobulicium, a monotypic genus with a distinct morphology of seven-lobed basidiospores, was placed as sister to the rest of Atheliales. A new family is proposed to accommodate this genus, Lobuliciaceae fam. nov. The remaining four lineages can be named following the family-level classification by Jülich (1982), and thus we opted to use the names Atheliaceae, Byssocorticiaceae, Pilodermataceae, and Tylosporaceae, albeit with amended circumscriptions.

ARBitR: an overlap-aware genome assembly scaffolder for linked reads.

SUMMARY: Linked genomic sequencing reads contain information that can be used to join sequences together into scaffolds in draft genome assemblies. Existing software for this purpose performs the scaffolding by joining sequences with a gap between them, not considering potential overlaps of contigs. We developed ARBitR to create scaffolds where overlaps are taken into account and show that it can accurately recreate regions where draft assemblies are broken. AVAILABILITY AND IMPLEMENTATION: ARBitR is written and implemented in Python3 for Unix-based operative systems. All source code is available at https://github.com/markhilt/ARBitR under the GNU General Public License v3. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Morphology, Multilocus Phylogeny, and Toxin Analysis Reveal Amanita albolimbata, the First Lethal Amanita Species From Benin, West Africa.

Many species of Amanita sect. Phalloideae (Fr.) Quél. cause death of people after consumption around the world. Amanita albolimbata, a new species of A. sect. Phalloideae from Benin, is described here. The taxon represents the first lethal species of A. sect. Phalloideae known from Benin. Morphology and molecular phylogenetic analyses based on five genes (ITS, nrLSU, rpb2, tef1-α, and ß-tubulin) revealed that A. albolimbata is a distinct species. The species is characterized by its smooth, white pileus sometimes covered by a patchy volval remnant, a bulbous stipe with a white limbate volva, broadly ellipsoid to ellipsoid, amyloid basidiospores, and abundant inflated cells in the volva. Screening for the most notorious toxins by liquid chromatography-high-resolution mass spectrometry revealed the presence of α-amanitin, ß-amanitin, and phallacidin in A. albolimbata.

Naming the untouchable - environmental sequences and niche partitioning as taxonomical evidence in fungi.

Due to their submerged and cryptic lifestyle, the vast majority of fungal species are difficult to observe and describe morphologically, and many remain known to science only from sequences detected in environmental samples. The lack of practices to delimit and name most fungal species is a staggering limitation to communication and interpretation of ecology and evolution in kingdom Fungi. Here, we use environmental sequence data as taxonomical evidence and combine phylogenetic and ecological data to generate and test species hypotheses in the class Archaeorhizomycetes (Taphrinomycotina, Ascomycota). Based on environmental amplicon sequencing from a well-studied Swedish pine forest podzol soil, we generate 68 distinct species hypotheses of Archaeorhizomycetes, of which two correspond to the only described species in the class. Nine of the species hypotheses represent 78% of the sequenced Archaeorhizomycetes community, and are supported by long read data that form the backbone for delimiting species hypothesis based on phylogenetic branch lengths.Soil fungal communities are shaped by environmental filtering and competitive exclusion so that closely related species are less likely to co-occur in a niche if adaptive traits are evolutionarily conserved. In soil profiles, distinct vertical horizons represent a testable niche dimension, and we found significantly differential distribution across samples for a well-supported pair of sister species hypotheses. Based on the combination of phylogenetic and ecological evidence, we identify two novel species for which we provide molecular diagnostics and propose names. While environmental sequences cannot be automatically translated to species, they can be used to generate phylogenetically distinct species hypotheses that can be further tested using sequences as ecological evidence. We conclude that in the case of abundantly and frequently observed species, environmental sequences can support species recognition in the absences of physical specimens, while rare taxa remain uncaptured at our sampling and sequencing intensity.

Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi.

With ∼36,000 described species, Agaricomycetes are among the most successful groups of Fungi. Agaricomycetes display great diversity in fruiting body forms and nutritional modes. Most have pileate-stipitate fruiting bodies (with a cap and stalk), but the group also contains crust-like resupinate fungi, polypores, coral fungi, and gasteroid forms (e.g., puffballs and stinkhorns). Some Agaricomycetes enter into ectomycorrhizal symbioses with plants, while others are decayers (saprotrophs) or pathogens. We constructed a megaphylogeny of 8,400 species and used it to test the following five hypotheses regarding the evolution of morphological and ecological traits in Agaricomycetes and their impact on diversification: 1) resupinate forms are plesiomorphic, 2) pileate-stipitate forms promote diversification, 3) the evolution of gasteroid forms is irreversible, 4) the ectomycorrhizal (ECM) symbiosis promotes diversification, and 5) the evolution of ECM symbiosis is irreversible. The ancestor of Agaricomycetes was a saprotroph with a resupinate fruiting body. There have been 462 transitions in the examined morphologies, including 123 origins of gasteroid forms. Reversals of gasteroid forms are highly unlikely but cannot be rejected. Pileate-stipitate forms are correlated with elevated diversification rates, suggesting that this morphological trait is a key to the success of Agaricomycetes. ECM symbioses have evolved 36 times in Agaricomycetes, with several transformations to parasitism. Across the entire 8,400-species phylogeny, diversification rates of ectomycorrhizal lineages are no greater than those of saprotrophic lineages. However, some ECM lineages have elevated diversification rates compared to their non-ECM sister clades, suggesting that the evolution of symbioses may act as a key innovation at local phylogenetic scales.

When mycologists describe new species, not all relevant information is provided (clearly enough).

Taxonomic mycology struggles with what seems to be a perpetual shortage of resources. Logically, fungal taxonomists should therefore leverage every opportunity to highlight and visualize the importance of taxonomic work, the usefulness of taxonomic data far beyond taxonomy, and the integrative and collaborative nature of modern taxonomy at large. Is mycology really doing that, though? In this study, we went through ten years' worth (2009-2018) of species descriptions of extant fungal taxa - 1,097 studies describing at most ten new species - in five major mycological journals plus one plant journal. We estimated the frequency at which a range of key words, illustrations, and concepts related to ecology, geography, taxonomy, molecular data, and data availability were provided with the descriptions. We also considered a range of science-demographical aspects such as gender bias and the rejuvenation of taxonomy and taxonomists as well as public availability of the results. Our results show that the target audience of fungal species descriptions appears to be other fungal taxonomists, because many aspects of the new species were presented only implicitly, if at all. Although many of the parameters we estimated show a gradual, and in some cases marked, change for the better over time, they still paint a somewhat bleak picture of mycological taxonomy as a male-dominated field where the wants and needs of an extended target audience are often not understood or even considered. This study hopes to leave a mark on the way fungal species are described by putting the focus on ways in which fungal taxonomy can better anticipate the end users of species descriptions - be they mycologists, other researchers, the public at large, or even algorithms. In the end, fungal taxonomy, too, is likely to benefit from such measures.

The genus Catathelasma (Catathelasmataceae, Basidiomycota) in China.

Two new species, Catathelasma laorentou and C. subalpinum, are described on the basis of morphological characters, phylogenetic evidence, host preferences and geographic distributions. A taxonomic key to the known species in China is also provided to facilitate identification. Based on samples from temperate Asia, Europe and North America, the phylogeny of Catathelasma was reconstructed using the internal transcribed spacer (ITS) region, the large subunit (LSU) of the ribosomal DNA and the translation elongation factor 1-α (TEF1).The phylogenetic results showed that Catathelasma contains two monophyletic clades: the /subalpinum clade and the /imperiale clade. The Asian species C. laorentou and C. subalpinum are closely related to the North American C. sp. (labelled as C. ventricosum in GenBank) in the /subalpinum clade, whereas C. imperiale and C. singeri are closely related in the /imperiale clade.

Maintenance of High Genome Integrity over Vegetative Growth in the Fairy-Ring Mushroom Marasmius oreades.

Most mutations in coding regions of the genome are deleterious, causing selection to favor mechanisms that minimize the mutational load over time [1-5]. DNA replication during cell division is a major source of new mutations. It is therefore important to limit the number of cell divisions between generations, particularly for large and long-lived organisms [6-9]. The germline cells of animals and the slowly dividing cells in plant meristems are adaptations to control the number of mutations that accumulate over generations [9-11]. Fungi lack a separated germline while harboring species with very large and long-lived individuals that appear to maintain highly stable genomes within their mycelia [8, 12, 13]. Here, we studied genomic mutation accumulation in the fairy-ring mushroom Marasmius oreades. We generated a chromosome-level genome assembly using a combination of cutting-edge DNA sequencing technologies and re-sequenced 40 samples originating from six individuals of this fungus. The low number of mutations recovered in the sequencing data suggests the presence of an unknown mechanism that works to maintain extraordinary genome integrity over vegetative growth in M. oreades. The highly structured growth pattern of M. oreades allowed us to estimate the number of cell divisions leading up to each sample [14, 15], and from this data, we infer an incredibly low per mitosis mutation rate (3.8 × 10-12 mutations per site and cell division) as one of several possible explanations for the low number of identified mutations.

Structure and function of the global topsoil microbiome.

Soils harbour some of the most diverse microbiomes on Earth and are essential for both nutrient cycling and carbon storage. To understand soil functioning, it is necessary to model the global distribution patterns and functional gene repertoires of soil microorganisms, as well as the biotic and environmental associations between the diversity and structure of both bacterial and fungal soil communities1-4. Here we show, by leveraging metagenomics and metabarcoding of global topsoil samples (189 sites, 7,560 subsamples), that bacterial, but not fungal, genetic diversity is highest in temperate habitats and that microbial gene composition varies more strongly with environmental variables than with geographic distance. We demonstrate that fungi and bacteria show global niche differentiation that is associated with contrasting diversity responses to precipitation and soil pH. Furthermore, we provide evidence for strong bacterial-fungal antagonism, inferred from antibiotic-resistance genes, in topsoil and ocean habitats, indicating the substantial role of biotic interactions in shaping microbial communities. Our results suggest that both competition and environmental filtering affect the abundance, composition and encoded gene functions of bacterial and fungal communities, indicating that the relative contributions of these microorganisms to global nutrient cycling varies spatially.