Biology subjects

Macias, A. M.

Publications and source records attributed to Macias, A. M..

5 recordsLinked to original sources

bioRxiv2024

More fungi than legs: the first fungal microbiome for a fungus-eating millipede (Colobognatha)

Fungi are widely consumed across the animal kingdom for nutritional and defensive benefits. Millipedes, among the first air-breathing land animals, were also among the first terrestrial fungivores. As detritus-eating omnivores, most millipedes regularly consume fungi. Millipede diets diverged [~]200 million years ago, when obligate fungivorous millipedes (subterclass Colobognatha) diverged from their detritivorous counterparts. Despite their global distribution and uncommon diet, little is known about the association between Colobognaths and the fungi they consume. In 2019, surveys of fungal communities associated with the Colobognath Brachycybe lecontii revealed associations with at least 176 genera of culturable fungi. Given the known biases of culture-based approaches, a more comprehensive survey of B. lecontiis fungal microbiome using amplicon sequencing was undertaken. In this study, we generated amplicon sequence data to look for associations between fungi and B. lecontii, and to determine if patterns of fungal diversity are millipede- or habitat-driven. Altogether, the fungal microbiome of B. lecontii encompassed 620 fungal genera and 100 orders. Despite much greater observed fungal diversity in the amplicon-based study, sampling was likely not sufficient to capture the full diversity of fungi associated with B. lecontii. Taxonomic and functional diversity were significantly influenced by site and colony, indicating that community structure is shaped by geography and habitat. It remains unknown whether these findings are representative of the larger patterns of fungal diversity for the entire millipede subterclass. Nevertheless, the obligate fungivorous lifestyle employed by these long-extant animals may provide important clues regarding fungal diversity and function.

microbiology↗

bioRxiv2023

Signatures of transposon-mediated genome inflation, host specialization, and photoentrainment in Entomophthora muscae and allied entomophthoralean fungi

Despite over a century of observations, the obligate insect parasites within the order Entomophthorales remain poorly characterized at the genetic level. This is in part due to their large genome sizes and difficulty in obtaining sequenceable material. In this manuscript, we leveraged a recently-isolated, laboratory-tractable Entomophthora muscae isolate and improved long-read sequencing to obtain a largely-complete entomophthoralean genome. Our E. muscae assembly is 1.03 Gb, consists of 7,810 contigs and contains 81.3% complete fungal BUSCOs. Using a comparative approach with other available (transcriptomic and genomic) datasets from entomophthoralean fungi, we provide new insight into the biology of these understudied pathogens. We offer a head-to-head comparison of morphological and molecular data for species within the E. muscae species complex. Our findings suggest that substantial taxonomic revision is needed to define species within this group and we provide recommendations for differentiating strains and species in the context of the existing body of E. muscae scientific literature. We show that giant genomes are the norm within Entomophthoraceae owing to extensive, but not recent, Ty3 retrotransposon activity, despite the presence of machinery to defend against transposable elements(RNAi). In addition, we find that E. muscae and its closest allies are enriched for M16A peptidases and possess genes that are likely homologs to the blue-light sensor white-collar 1, a Neurospora crassa gene that has a well-established role in maintaining circadian rhythms. We find that E. muscae has an expanded group of acid-trehalases, consistent with trehalose being the primary sugar component of fly (and insect) hemolymph. We uncover evidence that E. muscae diverged from other entomophthoralean fungi by expansion of existing families, rather than loss of particular domains, and possesses a potentially unique suite of secreted catabolic enzymes, consistent with E. muscaes species-specific, biotrophic lifestyle. Altogether, we provide a genetic and molecular foundation that we hope will provide a platform for the continued study of the unique biology of entomophthoralean fungi.

genomics↗

bioRxiv2019

Evolutionary relationships among Massospora spp. (Entomophthorales), obligate pathogens of cicadas

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 ecology of Massospora, much about its host range and diversity remains unexplored. The emerging phylogenetic framework can provide a foundation for exploring co-evolutionary relationships with cicada hosts and the evolution of behavior-altering compounds.

microbiology↗

bioRxiv2019

Diversity and function of fungi associated with the fungivorous millipede, Brachycybe lecontii

Fungivorous millipedes (subterclass Colobognatha) likely represent some of the earliest known mycophagous terrestrial arthropods, yet their fungal partners remain elusive. Here we describe relationships between fungi and the fungivorous millipede, Brachycybe lecontii. Their fungal community is surprisingly diverse with 176 genera, 39 orders, and four phyla and includes several undescribed species. Of particular interest are twelve genera conserved across wood substrates and millipede clades that comprise the core fungal community of B. lecontii. Wood decay fungi, long speculated to serve as the primary food source for Brachycybe species, were absent from this core assemblage and proved lethal to millipedes in pathogenicity assays while entomopathogenic Hypocreales were more common in the core but had little effect on millipede health. This study represents the first survey of fungal communities associated with any colobognath millipede, and these results offer a glimpse into the complexity of millipede fungal communities.

microbiology↗

bioRxiv2018

Discovery of psychoactive plant and mushroom alkaloids in ancient fungal cicada pathogens

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.

ecology↗