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.
The fungal genus Massospora (Zoopagomycota: Entomophthorales) includes more than a dozen obligate, sexually transmissible pathogenic species that infect cicadas (Hemiptera) worldwide. At least two species are known to produce psychoactive compounds during infection, which has garnered considerable interest for this enigmatic genus. As with many Entomophthorales, the evolutionary relationships and host associations of Massospora spp. are not well understood. The acquisition of M. diceroproctae from Arizona, M. tettigatis from Chile, and M. platypediae from California and Colorado provided an opportunity to conduct molecular phylogenetic analyses and morphological studies to investigate if these fungi represent a monophyletic group and delimit species boundaries. In a three-locus phylogenetic analysis including the D1-D2 domains of the nuclear 28S rRNA gene (28S), elongation factor 1 alpha-like (EFL), and beta-tubulin (BTUB), Massospora was resolved in a strongly supported monophyletic group containing four well-supported genealogically exclusive lineages, based on two of three methods of phylogenetic inference. There was incongruence among the single-gene trees: two methods of phylogenetic inference recovered trees with either the same topology as the 3-gene concatenated tree (EFL), or a basal polytomy (28S, BTUB). Massospora levispora and M. platypediae isolates formed a single lineage in all analyses and are synonymized here as M. levispora. Massospora diceroproctae was sister to M. cicadina in all three single-gene trees and on an extremely long branch relative to the other Massospora, and even the outgroup taxa, which may reflect an accelerated rate of molecular evolution and/or incomplete taxa sampling. The results of the morphological study presented here indicate that spore measurements may not be phylogenetically or diagnostically informative. Despite recent advances in understanding the
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.
The objective of the current study was to determine if age, diet, and genetic disposition (animal strain) in an animal model had early effects on specific molecular markers in circulating peripheral blood mononuclear cells (PBMCs). Three strains [Sprague-Dawley (SD), Fischer 344 (F344), and Brown-Norway (BN)] of male rats were maintained on a high-fat (HF) or regular diet. Blood was collected at 4, 12, and 24 wk to assess chemistry and to recover PBMCs. Triglycerides and body weight gain increased at all time points in the HF diet group for each strain. Telomere length in PBMCs decreased in the HF diet group compared to the regular diet group up to 24 wk in all strains. Telomere length decreased in PBMCs at 24 wk compared to baseline in all strains, indicating an age-related effect. These findings highlight that diet and age cause changes in PBMCs recovered from different strains of rats. The next tier of studies will examine the contribution of an occupational exposure (e.g., welding fume inhalation) in combination with diet, age, and strain, to assess changes in the molecular responses of isolated PBMCs. In addition, studies involving lifestyle exposure (e.g., tobacco smoke) are in the planning stages and will assess the long-term effects of exposure in our animal model.
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