An Improved 1.5-Gigabase Draft Assembly of Massospora cicadina (Zoopagomycota), an Obligate Fungal Parasite of 13- and 17-Year Cicadas

Stajich, Jason E.; Lovett, Brian; Ettinger, Cassandra L.; Carter-House, Derreck; Kurbessoian, Tania; Kasson, Matthew T.

doi:10.1128/mra.00367-22

Cited by 9 publications

(9 citation statements)

References 39 publications

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“…Fungi play diverse ecological roles and interact with various organisms in both terrestrial and aquatic environments ( James, Kauff, et al 2006 ; Stajich et al 2009 ; Spatafora et al 2017 ; Fisher et al 2020 ). Since their divergence from a common ancestor with animals over 1 billion years ago, fungi have evolved complex relationships with other organisms, including animals, bacteria, plants, protists, and other fungi ( Currie et al 2003 ; Frey-Klett et al 2011 ; Parfrey et al 2011 ; Gruninger et al 2014 ; Uehling et al 2017 ; Wang et al 2018 ; Chambouvet et al 2019 ; Malar et al 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Wang

Chang

Ortañez

et al. 2023

Genome Biology and Evolution

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Fungi have evolved over millions of years and their species diversity is predicted to be the second largest on the earth. Fungi have cross-kingdom interactions with many organisms which have mutually shaped their evolutionary trajectories. Zygomycete fungi hold a pivotal position in the fungal tree of life and provide important perspectives on the early evolution of fungi from aquatic to terrestrial environments. Phylogenomic analyses have found that zygomycete fungi diversified into two separate clades, the Mucoromycota which are frequently associated with plants and Zoopagomycota that are commonly animal-associated fungi. Genetic elements that contributed to the fitness and divergence of these lineages may have been shaped by the varied interactions these fungi have had with plants, animals, bacteria and other microbes. To investigate this, we performed comparative genomic analyses of the two clades of zygomycetes in the context of Kingdom Fungi, benefiting from our generation of a new collection of zygomycete genomes, including nine produced for this study. We identified lineage-specific genomic content which may contribute to the disparate biology observed in these zygomycetes. Our findings include the discovery of undescribed diversity in CotH, a Mucormycosis pathogenicity factor, which was found in a broad set of zygomycetes. Reconciliation analysis identified multiple duplication events and an expansion of CotH copies throughout the Mucoromycotina, Mortierellomycotina, Neocallimastigomycota, and Basidiobolus lineages. A kingdom-level phylogenomic analysis also identified new evolutionary relationships within the sub-phyla of Mucoromycota and Zoopagomycota, including supporting the sister-clade relationship between Glomeromycotina and Mortierellomycotina and the placement of Basidiobolus as sister to other Zoopagomycota lineages.

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Section: Introductionmentioning

confidence: 99%

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Wang

Chang

Ortañez

et al. 2023

Genome Biology and Evolution

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“…To glean biological insights from this new genome, we used a comparative approach to place our new genome in the context of other newly-available entomophthoralean data. We collated a dataset consisting of the latest available genomic and transcriptomic data for entomophthoralean fungi, including genomes for the specialist pathogens E. muscae (this study), Entomophaga maimaiga (ARSEF 7190 v1.0) and Massospora cicadina (Stajich JE. et al, 2022), transcriptomes for the specialists Pandora formicae (Małagocka et al, 2015) and Strongwellsea castrans (this study) and genomes for the generalists Zoophthora radicans (Amses et al, 2022), Neoconidiobolus thromboides (Chang et al, 2022) and C. coronatus (NRRL 28638; Fig.…”

Section: Resultsmentioning

confidence: 99%

Signatures of transposon-mediated genome inflation, host specialization, and photoentrainment inEntomophthora muscaeand allied entomophthoralean fungi

Stajich,

Lovett,

Lee

et al. 2023

Preprint

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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 anti-transposable element defense machinery (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.

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“… Massospora cicadina (Zoopagomycota) is an understudied obligate entomopathogenic fungus that infects periodical cicadas ( 1 , 2 ). During assembly and annotation of an improved genomic resource for M. cicadina strain MCPNR19 (ARSEF 14555) ( 3 ) using BlobTools2 ( 4 ), we identified many bacterial contigs. Given the discovery of psychoactive compounds present in Massospora species ( 5 ) and the uncertainty regarding their production, coupled with the established relationships between cicadas and bacterial mutualists ( 6 ), we sought to bin metagenome-assembled genomes (MAGs) from the improved M. cicadina genome to inform future investigations into tripartite cicada- Massospora -bacteria interactions.…”

Section: Announcementmentioning

confidence: 99%

“…The sampling, extraction, sequencing, quality control, and assembly methods are described by Stajich et al ( 3 ). Briefly, conidia and azygospores of M. cicadina MCPNR19 (ARSEF 14555) were collected from fungal plugs of infected brood XIII Pharaoh cicadas ( Magicicada septendecim ) in June 2019.…”

Section: Announcementmentioning

confidence: 99%

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Metagenome-Assembled Genomes of Bacteria Associated with Massospora cicadina Fungal Plugs from Infected Brood VIII Periodical Cicadas

Ettinger

Lovett

Kasson

et al. 2022

Microbiol Resour Announc

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We report six metagenome-assembled genomes (MAGs) associated with Massospora cicadina strain MCPNR19 (ARSEF 14555), an obligate entomopathogenic fungus of periodical cicadas. The MAGs include representatives of Pantoea , Pseudomonas , Lactococcus , and one potential new Chryseobacterium species. Future research is needed to resolve the ecology of these MAGs and determine whether they represent symbionts or contaminants.

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An Improved 1.5-Gigabase Draft Assembly of Massospora cicadina (Zoopagomycota), an Obligate Fungal Parasite of 13- and 17-Year Cicadas

Abstract: A 1.488-Gb draft genome sequence was assembled for the fungus Massospora cicadina , an obligate parasite of periodical cicadas. The M. cicadina genome has experienced massive expansion via transposable elements (TEs), which account for 92% of the genome.

Cited by 9 publications

References 39 publications

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Divergent Evolution of Early Terrestrial Fungi Reveals the Evolution of Mucormycosis Pathogenicity Factors

Signatures of transposon-mediated genome inflation, host specialization, and photoentrainment inEntomophthora muscaeand allied entomophthoralean fungi

Metagenome-Assembled Genomes of Bacteria Associated with Massospora cicadina Fungal Plugs from Infected Brood VIII Periodical Cicadas

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