Biology subjects

Matheny, P. B.

Publications and source records attributed to Matheny, P. B..

4 recordsLinked to original sources

bioRxiv2021

Evolutionary priming and transition to the ectomycorrhizal habit in an iconic lineage of mushroom-forming fungi: is preadaptation a requirement?

The ectomycorrhizal symbiosis is an essential guild of many forested ecosystems and has a dynamic evolutionary history across kingdom Fungi, having independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic features of the transition to the ectomycorrhizal habit within the Russulaceae, one of the most diverse lineages of ectomycorrhizal fungi. We present comparative analyses of the pangenome and gene repertoires of 21 species across the order Russulales, including a closely related saprotrophic member of Russulaceae. The ectomycorrhizal Russulaceae is inferred to have originated around the Cretaceous-Paleogene extinction event (73.6-60.1 million years ago (MY)). The genomes of the ectomycorrhizal Russulaceae are characterized by a loss of genes for plant cell-wall degrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of genes coding for certain secreted proteins with TE "nests". The saprotrophic sister group of the ectomycorrhizal Russulaceae, Gloeopeniophorella convolvens, possesses some of these aspects (e.g., loss of some PCWDE and protease orthologs, TE expansion, reduction in secondary metabolism clusters), resulting from an accelerated rate of gene evolution in the shared ancestor of Russulaceae that predates the evolution of the ectomycorrhizal habit. Genomes of Russulaceae possess a high degree of synteny, including a conserved set of terpene secondary metabolite gene clusters. We hypothesize that the evolution of the ectomycorrhizal habit requires premodification of the genome for plant root association followed by an accelerated rate of gene evolution within the secretome for host-defense circumvention and symbiosis establishment.

evolutionary biology↗

bioRxiv2019

Miocene and Pliocene speciation of Russula subsection Roseinae in temperate forests of eastern North America

Numerous lineages of mushroom-forming fungi have been subject to bursts of diversification throughout their evolutionary history, events that can impact our ability to infer well-resolved phylogenies. However, groups that have undergone quick genetic change may have the highest adaptive potential. As the second largest genus of mushroom-forming fungi, Russula provides an excellent model for studying hyper-diversification and processes in evolution that drives it. This study focuses on the morphologically defined group - Russula subsection Roseinae. Species hypotheses based on morphological differentiation and multi-locus phylogenetic analyses are tested in the Roseinae using different applications of the multi-species coalescent model. Based on this combined approach, we recognize fourteen species in Roseinae including the Albida and wholly novel Magnarosea clades. Reconstruction of biogeographic and host association history suggest that parapatric speciation in refugia during glacial cycles of the Pleistocene drove diversification within the Roseinae, which is found to have a Laurasian distribution with an evolutionary origin in the Appalachian Mountains of eastern North America. Finally, we detect jump dispersal at a continental scale that has driven diversification since the most recent glacial cycles.

evolutionary biology↗

bioRxiv2018

Phylogenomics reveals dynamic evolution of fungal nitric oxide reductases and their relationship to secondary metabolism

Fungi expressing P450nor, an unconventional nitric oxide (NO) reducing cytochrome P450, are thought to be significant contributors to soil nitrous oxide (N2O) emissions. However, fungal contributions to N2O emissions remain uncertain due to inconsistencies in measurements of N2O formation by fungi. Much of the N2O emitted from antibiotic-amended soil microcosms is attributed to fungal activity, yet fungal isolates examined in pure culture are poor N2O producers. To assist in reconciling these conflicting observations and produce a benchmark genomic analysis of fungal denitrifiers, genes underlying fungal denitrification were examined in >700 fungal genomes. Of 167 p450nor-containing genomes identified, 0, 30, and 48 also harbored the denitrification genes narG, napA or nirK, respectively. Compared to napA and nirK, p450nor was twice as abundant and exhibited two to five-fold more gene duplications, losses, and transfers, indicating a disconnect between p450nor presence and denitrification potential. Furthermore, co-occurrence of p450nor with genes encoding NO-detoxifying flavohemoglobins (Spearman r = 0.87, p = 1.6e-10) confounds hypotheses regarding P450nors primary role in NO detoxification. Instead, ancestral state reconstruction united P450nor with actinobacterial cytochrome P450s (CYP105) involved in secondary metabolism (SM) and 19 (11 %) p450nor-containing genomic regions were predicted to be SM clusters. Another 40 (24 %) genomes harbored genes nearby p450nor predicted to encode hallmark SM functions, providing additional contextual evidence linking p450nor to SM. These findings underscore the potential physiological implications of widespread p450nor gene transfer, support the novel affiliation of p450nor with fungal SM, and challenge the hypothesis of p450nors primary role in denitrification.

microbiology↗

bioRxiv2017

Horizontal gene cluster transfer increased hallucinogenic mushroom diversity

Secondary metabolites are heterogeneous natural products that often mediate interactions between species. The tryptophan-derived secondary metabolite, psilocin, is a serotonin receptor agonist that induces altered states of consciousness. A phylogenetically disjunct group of mushroom-forming fungi in the Agaricales produce the psilocin prodrug, psilocybin. Spotty phylogenetic distributions of fungal compounds are sometimes explained by horizontal transfer of metabolic gene clusters among unrelated fungi with overlapping niches. We report the discovery of a psilocybin gene cluster in three hallucinogenic mushroom genomes, and evidence for its horizontal transfer between fungal lineages. Patterns of gene distribution and transmission suggest that psilocybin provides a fitness advantage in the dung and late wood-decay niches, which may be reservoirs of fungal indole-based metabolites that alter behavior of mycophagous and wood-eating invertebrates. These hallucinogenic mushroom genomes will serve as models in neurochemical ecology, advancing the prospecting and synthetic biology of novel neuropharmaceuticals.

evolutionary biology↗