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1. Improved systematics of lorikeets reflects their evolutionary history and frames conservation priorities

   https://doi.org/10.1080/01584197.2020.1779596  

   Joseph, Leo; Merwin, Jon; Smith, Brian Tilston (July 2020, Emu)

   A well-supported genus-level classification of any group of organisms underpins downstream understanding of its evolutionary biology and enhances the role of phylogenetic diversity in guiding its conservation and management. The lorikeets (Psittaciformes: Loriini) are parrots for which genus-level systematics (phylogenetic relationships and classification) has long been unstable and unsatisfactory. Instability has manifested through frequently changing compositions of some genera (e.g. Trichoglossus and Psitteuteles). Other genera (e.g. Charmosyna, Vini) have become so large that their phenotypic heterogeneity alone at least questions whether they are monophyletic assemblages that genera should comprise. Recent molecular phylogenetic and phenotypic studies have improved the framework with which to rationalise genus-level systematics in lorikeets but some trenchant uncertainty has remained. Here we utilise published genomic data and tetrahedral analysis of plumage colour to develop a full review of the genus-level classification of lorikeets. Using existing phylogenetic relationships and a newly estimated time-calibrated tree for lorikeets, we show where paraphyletic assemblages have misled the classification of genera. We assign six species to three new genera and six other species to four previously described generic names that have been in synonymy in recent literature. Our taxonomic revision brings a new perspective informing and guiding the conservation and management of the lorikeets and their evolutionary biology. 

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2. Interactions among Escovopsis, Antagonistic Microfungi Associated with the Fungus-Growing Ant Symbiosis

   https://doi.org/10.3390/jof7121007  

   Christopher, Yuliana; Aguilar, Celestino; Gálvez, Dumas; Wcislo, William T.; Gerardo, Nicole M.; Fernández-Marín, Hermógenes (December 2021, Journal of Fungi)

   Fungi in the genus Escovopsis (Ascomycota: Hypocreales) are prevalent associates of the complex symbiosis between fungus-growing ants (Tribe Attini), the ants’ cultivated basidiomycete fungi and a consortium of both beneficial and harmful microbes found within the ants’ garden communities. Some Escovopsis spp. have been shown to attack the ants’ cultivated fungi, and co-infections by multiple Escovopsis spp. are common in gardens in nature. Yet, little is known about how Escovopsis strains impact each other. Since microbe–microbe interactions play a central role in microbial ecology and evolution, we conducted experiments to assay the types of interactions that govern Escovopsis–Escovopsis relationships. We isolated Escovopsis strains from the gardens of 10 attine ant genera representing basal (lower) and derived groups in the attine ant phylogeny. We conducted in vitro experiments to determine the outcome of both intraclonal and interclonal Escovopsis confrontations. When paired with self (intraclonal interactions), Escovopsis isolated from lower attine colonies exhibited antagonistic (inhibitory) responses, while strains isolated from derived attine colonies exhibited neutral or mutualistic interactions, leading to a clear phylogenetic pattern of interaction outcome. Interclonal interactions were more varied, exhibiting less phylogenetic signal. These results can serve as the basis for future studies on the costs and benefits of Escovopsis coinfection, and on the genetic and chemical mechanisms that regulate the compatibility and incompatibility observed here. 

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3. Genomic diversification of the specialized parasite of the fungus-growing ant symbiosis

   https://doi.org/10.1073/pnas.2213096119  

   Gotting, Kirsten; May, Daniel S.; Sosa-Calvo, Jeffrey; Khadempour, Lily; Francoeur, Charlotte B.; Berasategui, Aileen; Thairu, Margaret W.; Sandstrom, Shelby; Carlson, Caitlin M.; Chevrette, Marc G.; et al (December 2022, Proceedings of the National Academy of Sciences)

   Fungi shape the diversity of life. Characterizing the evolution of fungi is critical to understanding symbiotic associations across kingdoms. In this study, we investigate the genomic and metabolomic diversity of the genus Escovopsis , a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that Escovopsis forms a monophyletic group arising from a mycoparasitic fungal ancestor 61.82 million years ago (Mya). Across the evolutionary history of fungus-growing ants, the dates of origin of most clades of Escovopsis correspond to the dates of origin of the fungus-growing ants whose gardens they parasitize. We reveal that genome reduction, determined by both genomic sequencing and flow cytometry, is a consistent feature across the genus Escovopsis, largely occurring in coding regions, specifically in the form of gene loss and reductions in copy numbers of genes. All functional gene categories have reduced copy numbers, but resistance and virulence genes maintain functional diversity. Biosynthetic gene clusters (BGCs) contribute to phylogenetic differences among Escovopsis spp., and sister taxa in the Hypocreaceae. The phylogenetic patterns of co-diversification among BGCs are similarly exhibited across mass spectrometry analyses of the metabolomes of Escovopsis and their sister taxa. Taken together, our results indicate that Escovopsis spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis. 

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4. Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis

   https://doi.org/10.1128/AEM.00178-21  

   Francoeur, Charlotte B.; May, Daniel S.; Thairu, Margaret W.; Hoang, Don Q.; Panthofer, Olivia; Bugni, Tim S.; Pupo, Mônica T.; Clardy, Jon; Pinto-Tomás, Adrián A.; Currie, Cameron R. (June 2021, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis . Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies. IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis . The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia , is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis . 

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5. Phylogenomic analysis of the Neocallimastigomycota: Proposal of Caecomycetaceae fam. nov., Piromycetaceae fam. nov., and emended description of the families Neocallimastigaceae and Anaeromycetaceae

   RA Hanafy, Y Wang (January 2023, International journal of systematic and evolutionary microbiology)

   The anaerobic gut fungi (AGF) represent a coherent phylogenetic clade within the Mycota. Twenty genera have been described so far. Currently, the phylogenetic and evolutionary relationships between AGF genera remain poorly understood. Here, we utilized 52 transcriptomic datasets from 14 genera to resolve AGF inter-genus relationships using phylogenomics, and to provide a quantitative estimate (amino acid identity, AAI) for intermediate rank assignments. We identify four distinct supra-genus clades, encompassing all genera producing polyflagellated zoospores, bulbous rhizoids, the broadly circumscribed genus Piromyces, and the Anaeromyces and affiliated genera. We also identify the genus Khoyollomyces as the earliest evolving AGF genus. Concordance between phylogenomic outputs and RPB1 and D1/D2 LSU, but not RPB2, MCM7, EF1α, or ITS1, phylogenies was observed. We combine phylogenomic analysis, and AAI outputs with informative phenotypic traits to propose accommodating 14/20 AGF genera into four families: Caecomycetaceae fam. nov. (encompassing the genera Caecomyces and Cyllamyces), Piromycetaceae fam. nov. (encompassing the genus Piromyces), emend the description of fam. Neocallimastigaceae to encompass the genera Neocallimastix, Orpinomyces, Pecoramyces, Feramyces, Ghazallomyces, Aestipascuomyces, and Paucimyces, as well as the family Anaeromycetaceae to include the genera Oontomyces, Liebetanzomyces, and Capellomyces in addition to Anaeromyces. We refrain from proposing families for the deeply branching genus Khoyollomyces, and for genera with uncertain position (Buwchfawromyces, Joblinomyces, Tahromyces, Agriosomyces, and Aklioshbomyces) pending availability of additional isolates and sequence data; and these genera are designated as “genera incertae sedis” in the order Neocallimastigales. Our results establish an evolutionary-grounded Linnaean taxonomic framework for the AGF, provide quantitative estimates for rank assignments, and demonstrate the utility of RPB1 as an additional informative marker in Neocallimastigomycota taxonomy. 

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