Microsporidia and invertebrate hosts: genome-informed taxonomy surrounding a new lineage of crayfish-infecting Nosema spp. (Nosematida)

Abstract

The Microsporidia, an often overlooked fungal lineage, exhibit increasing diversity and taxonomic understanding with the use of genomic techniques. They are obligate parasites infecting a diversity of hosts, including crustaceans. Crustacea are, in essence, ancient insects and their relationship with the Microsporidia is both diverse and convoluted. Relationships between crayfish and their microsporidian parasites display geospatial and taxonomic diversity. Through classical (histological, ultrastructural, developmental) and genomic (phylogenetic, phylogenomic) approaches, we expand the known diversity of crayfish-infecting microsporidia into the genus Nosema by describing three novel species from North America: Nosema astafloridana n. sp. infecting Procambarus pictus and Procambarus spiculifer, Nosema rusticus n. sp. infecting Faxonius rusticus, and Nosema wisconsinii n. sp. infecting Faxonius propinquus and Faxonius virilis. Additionally, we provide SSU sequence data for further Nosema diversity from Procambarus clarkii and Pacifasticus gambelii. The taxonomy of aquatic crustacean-infecting Nosema have been under scrutiny among microsporidiologists—using genomic data we solidify this systematic relationship. Our genomic data reveal phylogenomic divergence between terrestrial insect-infecting Nosema and aquatic crustacean-infecting Nosema but place our novel species within the Nosema. Comparative genomic analysis reveal that Nosema rusticus n. sp. is a tetraploid organism, making this the first known polyploid from the genus Nosema. Annotation of the genomic data highlight that crayfish-infecting Nosema have distinct proteomic differences when compared to amphipod and insect-infecting microsporidians. Alongside the new diversity uncovered and genome-supported systematics, we consider the role of these new ‘invasive’ parasites in biological invasion systems, exploring their relationship with their invasive hosts.