Keaton Tremble

Dormancy is a key life history stage of many microbes that involves existence in a metabolically inactive state. Although dormant taxa may contribute little to community function, most microbial metabarcoding community surveys of microbial systems target DNA which captures dormant and dead taxa in addition to the active and living fraction of the community. RNA metabarcoding offers the potential to delineate the active fraction of microbial communities. Transitions between dormancy and activity may also serve as a rapid response mechanism for communities for communities to alter their function faster than turnover in community composition. Additionally, a focus on active microbiomes may provide further insight into which taxa should be prioritized as part of the core microbiome. We used DNA and RNA metabarcoding in samples collected as a time-series of the quaking aspen ( Populus tremuloides ) root microbiome across a natural environmental gradient to identify the degree of spatiotemporal dynamism in active and total microbial communities and to document the extent of dormancy in the core microbiome. We found that active bacterial and fungal communities were more temporally dynamic than total communities, while total communities exhibited a stronger response to spatial variability in site conditions. Additionally, we found that core microbiome members are frequently inactive, resulting in a reduced active core microbiome. This study stresses the need to focus on turnover in the active microbial community to detect variation in microbial communities in time-series and to use microbial activity levels as a key determinant of core microbiome membership.

The “magic mushroom” Psilocybe cubensis is cultivated worldwide for recreational and medicinal uses. Described initially from Cuba in 1904, there has been substantial debate about its origin and diversification. The prevailing view, first proposed by the Psilocybe expert Gastón Guzmán in 1983, is that P. cubensis was inadvertently introduced to the Americas when cattle were introduced to the continents from Africa and Europe (∼1500 CE), but that its progenitor was endemic to Africa. This hypothesis has never been tested. Here, we report the discovery of the closest wild relative of P. cubensis from sub-Saharan Africa, P. ochraceocentrata nom. prov. Using DNA sequences from type specimens of all known and accessable African species of Psilocybe , multi-locus phylogenetic and molecular clock analysis strongly support recognizing the African samples as a new species that last shared a common ancestor with P. cubensis ∼1.5 million years ago (∼710k - 2.55M years ago 95% HPD). Even at the latest estimated time of divergence, this long predates cattle domestication and the origin of modern humans. Both species are associated with herbivore dung, suggesting this habit likely predisposed P. cubensis to its present specialization on domesticated cattle dung. Ecological niche modeling using bioclimatic variables for global records of these species indicates historical presence across Africa, Asia, and the Americas over the last 3 million years. This discovery sheds light on the wild origins of domesticated P. cubensis and provides new genetic resources for research on psychedelic mushrooms.

Inbreeding, the mating of individuals that are related through common ancestry, is of central importance in evolutionary and conservation biology due to its impacts on individual fitness and population dynamics. However, while advanced genomic approaches have revolutionised the study of inbreeding in animals, genomic studies of inbreeding are rare in plants and lacking in fungi. We investigated global patterns of inbreeding in the prized edible porcini mushroom Boletus edulis using 225 whole genomes from seven lineages distributed across the northern hemisphere. Genomic inbreeding was quantified using runs of homozygosity (ROHs). We found appreciable variation both among and within lineages, with some individuals having over 20% of their genomes in ROHs. Much of this variation could be explained by a combination of elevation and latitude, and to a lesser extent by predicted habitat suitability during the last glacial maximum. In line with this, the majority of ROHs were short, reflecting ancient common ancestry dating back approximately 200–1700 generations ago, while longer ROHs indicative of recent common ancestry (less than approximately 50 generations ago) were infrequent. Our study reveals the inbreeding legacy of major climatic events in a widely distributed forest mutualist, aligning with prevailing theories and empirical studies of the impacts of historical glaciation events on the dominant forest tree species of the northern hemisphere.

The porcini mushroom family Boletaceae is a diverse, widespread group of ectomycorrhizal (ECM) mushroom-forming fungi that so far has eluded intrafamilial phylogenetic resolution based on morphology and multilocus data sets. In this study, we present a genome-wide molecular data set of 1764 single-copy gene families from a global sampling of 418 Boletaceae specimens. The resulting phylogenetic analysis has strong statistical support for most branches of the tree, including the first statistically robust backbone. The enigmatic Phylloboletellus chloephorus from non-ECM Argentinian subtropical forests was recovered as a new subfamily sister to the core Boletaceae. Time-calibrated branch lengths estimate that the family first arose in the early to mid-Cretaceous and underwent a rapid radiation in the Eocene, possibly when the ECM nutritional mode arose with the emergence and diversification of ECM angiosperms. Biogeographic reconstructions reveal a complex history of vicariance and episodic long-distance dispersal correlated with historical geologic events, including Gondwanan origins and inferred vicariance associated with its disarticulation. Together, this study represents the most comprehensively sampled, data-rich molecular phylogeny of the Boletaceae to date, establishing a foundation for future robust inferences of biogeography in the group.

The species-rich porcini mushroom family Boletaceae is a widespread and well-known group of ectomycorrhizal (ECM) mushroom-forming fungi that has eluded intrafamilial phylogenetic resolution despite many attempts using morphological traits and multi-locus molecular datasets. In this study, we present a genome-wide molecular dataset of 1764 single-copy gene families from a global sampling of 418 Boletaceae specimens. The resulting phylogenetic analysis has strong statistical support for most branches of the tree, including the first statistically robust backbone. The enigmatic Phylloboletellus chloephorus from non-ECM Argentinian subtropical forests was recovered as an early diverging lineage within the Boletaceae. Time-calibrated branch lengths estimate that the family first arose in the early- to mid-Cretaceous and underwent a rapid radiation in the Eocene, possibly when the ECM nutritional mode arose with the emergence and diversification of ECM angiosperms. Biogeographic reconstructions reveal a complex history of vicariance and episodic long-distance dispersal correlated with historical geologic events, including Gondwanan origins and cladogenesis patterns that parallel its fragmentation. Ancestral state reconstruction of sporocarp morphological traits predicts that the ancestor of the Boletaceae was lamellate with ornamented basidiospores, contrary to most contemporary “bolete” morphologies. Transition rates indicated that the lamellate hymenophore and sequestrate sporocarp are reversible traits. Together, this study represents the most comprehensively sampled, data-rich molecular phylogeny of the Boletaceae to date, enabling robust inferences of trait evolution and biogeography in the group.

Hybridization among diverged species is common across all domains of eukaryotic life, but appears to be particularly common in fungi. However, some fungi exhibit a greater tendency for hybridization than others and it is unclear what mechanisms facilitate or prevent hybridization. Here, we generated 253 whole genome sequences and 22 reference genomes within the globally distributed ectomycorrhizal species complex Boletus edulis Bull. and use a multi-faceted genomic approach to identify patterns of ongoing hybridization and determine whether hybridization is mediated by changes in genome structure, ecology, or both. We found that hybridization is common among species of B. edulis despite 2.1 million years of divergence. However, not all lineages that hybridize today exhibit patterns of introgression, indicating the presence of strong reproductive boundaries among some species. Using a pan-genomic approach we find that genome structural variation is abundant within B. edulis , but that the presence of ongoing introgression does not correlate with genome structural similarity or overall gene content. Instead, we find that the composition of ecologically relevant gene families more accurately predicts the presence of introgression among lineages and B. edulis as a group may specialize on chitin decomposition. Altogether, we show that ecological preferences are likely the primary driver of reproductive barriers in B. edulis .

In the hyperdiverse fungi, the process of speciation is virtually unknown, including for the > 20 000 species of ectomycorrhizal mutualists. To understand this process, we investigated patterns of genome-wide differentiation in the ectomycorrhizal porcini mushroom, Boletus edulis, a globally distributed species complex with broad ecological amplitude.By whole-genome sequencing 160 individuals from across the Northern Hemisphere, we genotyped 792 923 single nucleotide polymorphisms to characterize patterns of genome-wide differentiation and to identify the adaptive processes shaping global population structure.We show that B. edulis exhibits contrasting patterns of genomic divergence between continents, with multiple lineages present across North America, while a single lineage dominates Europe. These geographical lineages are inferred to have diverged 1.62-2.66 million years ago, during a period of climatic upheaval and the onset of glaciation in the Pliocene-Pleistocene boundary. High levels of genomic differentiation were observed among lineages despite evidence of substantial and ongoing introgression. Genome scans, demographic inference, and ecological niche models suggest that genomic differentiation is maintained by environmental adaptation, not physical isolation.Our study uncovers striking patterns of genome-wide differentiation on a global scale and emphasizes the importance of local adaptation and ecologically mediated divergence, rather than prezygotic barriers such as allopatry or genomic incompatibility, in fungal population differentiation.

Understanding the population processes and genetic mechanisms that give rise to new species remains one of the most elusive goals of modern evolutionary biology. In the hyperdiverse and ecologically important Fungi, the process of speciation is virtually unknown, including for the more than 20,000 species of obligate ectomycorrhizal mutualists that play essential roles in ecosystem function. We investigated patterns of genome-wide differentiation in the ectomycorrhizal porcini mushroom Boletus edulis, a globally distributed species complex with broad ecological amplitude. By whole genome sequencing 160 individuals from across the Northern Hemisphere, we identified 792,923 SNPs and used these to elucidate the demographic and adaptive processes shaping global population differentiation. We show that B. edulis exhibits deeply contrasting patterns of genomic divergence between continents, with multiple lineages being present across North America, while a single lineage dominates Europe over a vast geographic scale. These geographical lineages are inferred to have diverged between 2.66 and 1.62 million years ago, corresponding to a period of climatic upheaval and the onset of glaciation during the Pliocene-Pleistocene boundary. High levels of genomic differentiation were observed among lineages despite evidence of substantial and ongoing introgression. Furthermore, genome scans, demographic inference and ecological niche models all suggest that genomic differentiation is maintained by environmental adaptation and not physical isolation. Our study uncovers striking differences on a truly global scale and emphasizes the importance of local adaptation and ecologically mediated divergence, rather than prezygotic barriers such as allopatry or genomic incompatibility in population differentiation in Fungi.