Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina -infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora , which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora . The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.
Brachycybe (Wood) is a genus of fungivorous millipedes. To date, the fungal associates of these millipedes have never been characterized. In an attempt to resolve these relationships, culture-based approaches combined with DNA barcode sequencing were used. Sampling of 313 individuals collected from three of four B. lecontii clades and 20 sites across seven states uncovered at least 183 genera in 40 orders from four fungal phyla. At least seven putative new species were recovered in this study, despite the use of more classical culture-based approaches. Three of these fungi were phylogenetically resolved using ITS + LSU and include two new species, aff. Fonsecaea sp., Mortierella aff. ambigua, and a new genus related to Apophysomyces. Overall, the results of this study highlight the vast amount of undescribed fungal biodiversity associated with millipedes. Twelve fungal genera from nine orders showed high connectivity across the entire B. lecontii-associated fungal network, indicating a central role for these fungi in their association with these millipedes. These twelve include the two putative new species described above. The ecology of these and other fungal associates were also explored, using fungal cohort pairings and entomopathogenicity trials. Over 40% of all fungal pairings resulted in competitive interactions, a majority of which involved inhibition or overgrowth by fungi in the Hypocreales and Polyporales, respectively. The abundance of these competitive interactions in these two orders indicate differing ecological strategies. Hypocreales used chemical warfare to competitively exclude other fungi, while Polyporales physically overgrew their competitors. Mucoromycotan fungi used a similar strategy to the Polyporales. Results of a series of entomopathogenicity trials indicated that B. lecontii was less susceptible to entomopathogenic Hypocreales than an insect model (Galleria mellonella), even though these fungi are known to attack several classes of arthropods. Furthermore, the absence of a negative interaction between B. lecontii and entomopathogenic Hypocreales may indicate a beneficial relationship. When challenged with Polyporales, B. lecontii exhibited high mortality, while G. mellonella was unaffected. This stands in sharp contrast to previous casual observations of the feeding behavior of B. lecontii. Recent discoveries of previously overlooked fungal diversity have been groundbreaking and hint at substantial cryptic fungal biodiversity across the globe. The 200-300 million-year-old association between fungi and the Colobognatha, which includes Brachycybe lecontii, provides an ideal system to uncover biodiversity and examine function of these fungi in a highly understudied and ancient association.
Abstract:The success of some invasive tree species is attributed, in part, to high fecundity in the form of sexual propagules. If invasive trees produce more seed annually than co-occurring native trees, they will have a greater ability to disperse and establish across the landscape. In this study, seed production of female Ailanthus trees was investigated to determine (1) reproductive age limits; (2) annual and cumulative seed output; and (3) seed viability. Existing data on Ailanthus seed production were combined with a novel dataset to compare variability in seed production and explore relationships with tree diameter and age. Results from this study showed Ailanthus' reproductive window is exceptional, spanning more than a century, with seed viability exceeding 65% from a 104-year-old individual. Germination studies and complementary tetrazolium assays also confirmed high propagule viability from a 7-year-old Ailanthus and supports tetrazolium assays as a proxy for germination studies. Not only can individual Ailanthus produce >1 million seeds annually, but a significant relationship exists between seed production and tree diameter. Using this relationship, cumulative seed production in individual Ailanthus can reach ca. 10 and 52 million seeds over a 40-year and 100-year period, respectively. This study provides a comprehensive investigation of various facets of the reproductive potential of Ailanthus.
Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but select species keep insects alive while sporulating, which enhances dispersal. Transcriptomics and metabolomics studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses, yet mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which appear to represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.
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