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• W4281774004 abstract "Microsporidian systematics has entered a genomic era, with ~38 species’ genomes available to date, and this number is expected to double by the end of 2022.Minimal frameworks can unite microsporidian taxonomy, promoting global access to high-quality genetic/pathological data. We propose sequencing of the internal transcribed spacer (ITS), large-subunit (LSU) region, and small-subunit ribosomal RNA gene (SSU), in lieu of genomic data, when describing microsporidian taxa.Ecological parameters across formally described Microsporidia are synthesised, revealing astonishing ecological diversity, which is mapped to their phylogenetic clade-based higher taxonomy.We coalesce previous microsporidian taxonomic classifications with new-age clade-based systematics to draw parallels between classical taxonomic approaches for other organisms and the Microsporidia. Microsporidian diversity is vast. There is a renewed drive to understand how microsporidian pathological, genomic, and ecological traits relate to their phylogeny. We comprehensively sample and phylogenetically analyse 125 microsporidian genera for which sequence data are available. Comparing these results with existing phylogenomic analyses, we suggest an updated taxonomic framework to replace the inconsistent clade numbering system, using informal taxonomic names: Glugeida (previously clades 5/3), Nosematida (4a), Enterocytozoonida (4b), Amblyosporida (3/5), Neopereziida (1), and Ovavesiculida (2). Cellular, parasitological, and ecological traits for 281 well-defined species are compared with identify clade-specific patterns across long-branch Microsporidia. We suggest that future taxonomic circumscriptions of Microsporidia should involve additional markers (SSU/ITS/LSU), and that a comprehensive suite of phenotypic and ecological traits help to predict broad microsporidian functional and lineage diversity. Microsporidian diversity is vast. There is a renewed drive to understand how microsporidian pathological, genomic, and ecological traits relate to their phylogeny. We comprehensively sample and phylogenetically analyse 125 microsporidian genera for which sequence data are available. Comparing these results with existing phylogenomic analyses, we suggest an updated taxonomic framework to replace the inconsistent clade numbering system, using informal taxonomic names: Glugeida (previously clades 5/3), Nosematida (4a), Enterocytozoonida (4b), Amblyosporida (3/5), Neopereziida (1), and Ovavesiculida (2). Cellular, parasitological, and ecological traits for 281 well-defined species are compared with identify clade-specific patterns across long-branch Microsporidia. We suggest that future taxonomic circumscriptions of Microsporidia should involve additional markers (SSU/ITS/LSU), and that a comprehensive suite of phenotypic and ecological traits help to predict broad microsporidian functional and lineage diversity. Taxonomic and evolutionary history across the MicrosporidiaThe Microsporidia (see Glossary) are a group of human-, animal- and microeukaryote-infecting, obligate, spore-forming parasites, whose systematic framework has been in flux over the past century [1.Murareanu B.M. et al.Generation of a Microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of Microsporidia.mBio. 2021; 12e0149021Crossref PubMed Google Scholar]. Historically, the group has had a morphology/ecology-based taxonomy whereby their complex intracellular life cycle, unique morphological features, and host range (including tissue tropism) were used to provide taxonomic insight [2.Sprague V. Classification and phylogeny of the Microsporidia.in: Bulla L.A. Cheng T.C. Comparative Pathobiology. Springer, 1977: 1-30Crossref Google Scholar]. These features remain important, but molecular and genomic technologies are rapidly providing evidence to revise microsporidian systematics and ecological affiliations, becoming the gold standard for species identification and broader phylogenetic placement [1.Murareanu B.M. et al.Generation of a Microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of Microsporidia.mBio. 2021; 12e0149021Crossref PubMed Google Scholar,3.Wadi L. Reinke A.W. Evolution of Microsporidia: an extremely successful group of eukaryotic intracellular parasites.PLoS Pathog. 2020; 16e1008276Crossref PubMed Scopus (32) Google Scholar]. With these tools, we are beginning to unravel a more complete picture of microsporidian diversity and the role of microsporidians in ecological systems, including the indirect impacts of infection on host populations and their ecosystem services [4.Bojko J. Stentiford G.D. Microsporidian pathogens of aquatic animals.in: Reinke A.W. Weiss L. Microsporidia: Current Advances in Biology. Springer, 2022: 247-284Crossref Scopus (2) Google Scholar,5.Chauvet M. et al.Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem.Environ. Microbiol. 2022; 24: 1672-1686Crossref PubMed Scopus (2) Google Scholar].The Microsporidia are classified within the Opisthosporidia (Eukaryota: Opisthokonta) [6.Karpov S. et al.Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia.Front. Microbiol. 2014; 5: 1-11Crossref PubMed Scopus (139) Google Scholar,7.Adl S.M. et al.Revisions to the classification, nomenclature, and diversity of eukaryotes.J. Eukaryot. Microbiol. 2019; 66: 4-119Crossref PubMed Scopus (534) Google Scholar]. Early work using the small-subunit (SSU) rRNA gene for a large number of species to determine microsporidian phylogenies identified three environmentally defined groups (Aquasporidia, Marinosporidia, and Terresporidia), which were originally classified into five genetically distinct clades, sometimes referenced using Roman numerals (I, II, III, IV, V) and sometimes with Arabic numerals (1, 2, 3, 4, 5) [8.Vossbrinck C.R. Debrunner-Vossbrinck B.A. Molecular phylogeny of the Microsporidia: ecological, ultrastructural, and taxonomic considerations.Folia Parasitol. 2005; 52: 131-142Crossref PubMed Scopus (246) Google Scholar] – henceforth, we use Arabic numerals when referring to the clade-based taxonomy. Recently, multiple phylogenetic studies involving the long- and short-branch Microsporidia (including ‘Cryptomycota’) suggested an alternative configuration of clade numbers [9.Vossbrinck C.R. et al.Phylogeny of the Microsporidia.in: Weiss L. Becnel J. Microsporidia: Pathogens of Opportunity. Wiley, 2014: 203-220Crossref Scopus (44) Google Scholar,10.Bass D. et al.Clarifying the relationships between Microsporidia and Cryptomycota.J. Eukaryot. Microbiol. 2018; 18: 1282-1298Google Scholar], supported additional smaller clades or ‘orphan’ lineages [11.Dubuffet A. et al.A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems.Environ. Microbiol. 2021; 23: 4344-4359Crossref PubMed Scopus (9) Google Scholar,12.Park E. Poulin R. Revisiting the phylogeny of microsporidia.Int. J. Parasitol. 2021; 51: 855-864Crossref PubMed Scopus (9) Google Scholar], and presented a somewhat different configuration of the main five well-supported ‘clades’ (1, 3, 4a, 4b, 5) [12.Park E. Poulin R. Revisiting the phylogeny of microsporidia.Int. J. Parasitol. 2021; 51: 855-864Crossref PubMed Scopus (9) Google Scholar]. Within these clades are multiple microsporidian orders, containing ~45 families, ~218 genera, and an estimated ~1600 species [1.Murareanu B.M. et al.Generation of a Microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of Microsporidia.mBio. 2021; 12e0149021Crossref PubMed Google Scholar]. DNA sequence data are available for 125 (~55%) of the known genera. Metabarcoding, metagenomic, and other deposited genetic data suggest a much great diversity of microsporidians, predicting thousands of unknown or uncharacterised taxa [5.Chauvet M. et al.Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem.Environ. Microbiol. 2022; 24: 1672-1686Crossref PubMed Scopus (2) Google Scholar,11.Dubuffet A. et al.A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems.Environ. Microbiol. 2021; 23: 4344-4359Crossref PubMed Scopus (9) Google Scholar,13.Ardila-Garcia A.M. et al.Microsporidian diversity in soil, sand, and compost of the Pacific Northwest.J. Eukaryot. Microbiol. 2013; 60: 601-608Crossref PubMed Scopus (17) Google Scholar,14.Williams B.A.P. et al.Group-specific environmental sequencing reveals high levels of ecological heterogeneity across the microsporidian radiation.Environ. Microbiol. Rep. 2018; 10: 328-336Crossref PubMed Scopus (23) Google Scholar].The global diversity of microsporidians is only a small part of their story. These parasites play important roles in ecological systems [4.Bojko J. Stentiford G.D. Microsporidian pathogens of aquatic animals.in: Reinke A.W. Weiss L. Microsporidia: Current Advances in Biology. Springer, 2022: 247-284Crossref Scopus (2) Google Scholar,5.Chauvet M. et al.Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem.Environ. Microbiol. 2022; 24: 1672-1686Crossref PubMed Scopus (2) Google Scholar]. Over evolutionary time they have undergone extensive evolutionary reduction of their genomes and proteomes, resulting in metabolic dependence upon their hosts [15.Nakjang S. et al.Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics.Genome Biol. Evol. 2013; 5: 2285-2303Crossref PubMed Scopus (67) Google Scholar, 16.Wiredu-Boakye D. et al.Decay of the glycolytic pathway and adaptation to intranuclear parasitism within Enterocytozoonidae Microsporidia.Environ. Microbiol. 2017; 19: 2077-2089Crossref PubMed Scopus (46) Google Scholar, 17.Dean P. et al.Microsporidia: why make nucleotides if you can steal them?.PLoS Pathog. 2016; 12e1005870Crossref PubMed Scopus (39) Google Scholar, 18.Dean P. et al.Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites.Nat. Commun. 2018; 9: 1-12Crossref PubMed Scopus (31) Google Scholar]. Their physiologies confer specialised parasitological characteristics, including the potential to remain latent in hosts for many years [19.Kotkova M. et al.Latent microsporidiosis caused by Encephalitozoon cuniculi in immunocompetent hosts: a murine model demonstrating the ineffectiveness of the immune system and treatment with albendazole.PLoS One. 2013; 8e60941Crossref PubMed Scopus (53) Google Scholar], jumping host species [20.Ironside J.E. et al.Distribution and host range of the microsporidian Pleistophora mulleri.J. Eukaryot. Microbiol. 2008; 55: 355-362Crossref PubMed Scopus (16) Google Scholar], taking advantage of sex, cannibalism, and other host behaviours to transmit [21.Bunke M. et al.Parasites influence cannibalistic and predatory interactions within and between native and invasive amphipods.Dis. Aquat. Org. 2019; 136: 79-86Crossref PubMed Scopus (4) Google Scholar], persisting in the environment for long periods of time [22.Collado J.S. et al.Flow cytometry analysis of Nosema species to assess spore viability and longevity.Parasitol. Res. 2014; 113: 1695-1701Crossref PubMed Scopus (19) Google Scholar], and masking themselves from their hosts' immune defences [23.Bakowski M.A. et al.Ubiquitin-mediated response to Microsporidia and virus infection in C. elegans.PLoS Pathog. 2014; 10e1004200Crossref PubMed Scopus (109) Google Scholar,24.Reinke A.W. et al.Identification of Microsporidia host-exposed proteins reveals a repertoire of rapidly evolving proteins.Nat. Commun. 2017; 9: 14023Crossref Scopus (48) Google Scholar]. As pathogens, they pose a significant threat to humans, wildlife, and economically important species [25.Stentiford G.D. et al.Microsporidia–emergent pathogens in the global food chain.Trends Parasitol. 2016; 32: 336-348Abstract Full Text Full Text PDF PubMed Scopus (149) Google Scholar,26.Stentiford G.D. et al.Ultimate opportunists – the emergent Enterocytozoon group Microsporidia.PLoS Pathog. 2019; 15e1007668Crossref PubMed Scopus (23) Google Scholar].In this review, we gathered data from all microsporidian species with a formal taxonomic description that include genetic (partial/full-length SSU rRNA gene), pathological, and ultrastructural data (284 species, 125 genera). We generated a synthesis of multiple physiological and pathological traits and measurements across phylogenetic groups, including host and environmental information, to map microsporidian ecological relationships from across the globe (see Table S1 in the supplemental information online). The data are compared within and between each microsporidian clade to provide an assessment of any clade-scale ecological similarities and provide a discussion on shared traits and putative evolutionary and pathological relationships. We integrated information on evolutionary relationships from recent phylogenomic and SSU rRNA gene phylogenetic analyses, and several recent taxonomic revisions, some informed by intensive microsporidian-targeted environmental sequence diversity studies, to provide a phylogenetically informed name-based taxonomic structure, offering a strong framework for inevitable future discoveries of novel microsporidians infecting hosts from diverse environments.Taxonomy of canonical microsporidians: past, present, and futurePhylogenetics underpinning microsporidian taxonomyOur Bayesian SSU rRNA gene analysis includes a well-characterised representative species for all genera for which relevant sequence data exist (Figure 1, Key figure). The Bayesian topology also shows maximum-likelihood (ML) bootstrap values, which together confirm that the canonical Microsporidia comprises several relatively large and strongly supported subclades, and a smaller number of orphan lineages. Also included are sequences from key linages representing previously polyphyletic genera [e.g., Astathelohania (= Thelohania); Figure 2], whose sequences branched in different clades on the tree (Figure 1 and Table S1), but have recently been redescribed [27.Stratton C.E. et al.Revising the freshwater Thelohania to Astathelohania gen. et comb. nov., and description of two new species.Microorganisms. 2022; 10: 636Crossref PubMed Scopus (2) Google Scholar]. Such situations require revision by creating new genera for those lineages that do not correspond to the type taxon.Figure 2A comparison between the consensus genome tree topology from the most recent/comprehensively sampled phylogenomic analyses to our phylogenetic tree displayed in Figure 1 in the main text.Show full captionBoth trees are represented as cladograms in the figure, sporting a colour-coded system, which is labelled for the higher taxonomic group in which the members sit. The topology of the orthogroup cladogram was developed using Orthofinder (left) [63.Emms D.M. Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics.Genome Biol. 2019; 20: 1-14Crossref PubMed Scopus (1097) Google Scholar]; however, the support is based on existing genomic studies (right) [3.Wadi L. Reinke A.W. Evolution of Microsporidia: an extremely successful group of eukaryotic intracellular parasites.PLoS Pathog. 2020; 16e1008276Crossref PubMed Scopus (32) Google Scholar,54.Cormier A. et al.Draft genome sequences of Thelohania contejeani and Cucumispora dikerogammari, pathogenic microsporidia of freshwater crustaceans.Microbiol. Res. Announc. 2021; 10e01346-20PubMed Google Scholar]. The topology shows some complementarity; however, the position of some groups (Ovavesiculida, Glugeida, Amblyosporida, ‘orphan lineage’, and Neopereziida) branch differently relative to each other. The named clades as defined in this review are robustly recovered by both approaches, in some cases with stronger support in the phylogenomic analyses. Abbreviations: ML, maximum likelihood; SSU, small subunit.View Large Image Figure ViewerDownload Hi-res image Download (PPT)As for many SSU rRNA gene trees, the backbone of the tree is generally poorly resolved. The SSU gene does not provide enough phylogenetic signal to resolve these more ancient divergences. As more genomic datasets are generated for microsporidians, these relationships should become clearer via multigene phylogenomic analyses (Figure 2).Recent diversity studies and taxonomic revisions have advanced our view of microsporidian systematics [1.Murareanu B.M. et al.Generation of a Microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of Microsporidia.mBio. 2021; 12e0149021Crossref PubMed Google Scholar,5.Chauvet M. et al.Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem.Environ. Microbiol. 2022; 24: 1672-1686Crossref PubMed Scopus (2) Google Scholar,7.Adl S.M. et al.Revisions to the classification, nomenclature, and diversity of eukaryotes.J. Eukaryot. Microbiol. 2019; 66: 4-119Crossref PubMed Scopus (534) Google Scholar,9.Vossbrinck C.R. et al.Phylogeny of the Microsporidia.in: Weiss L. Becnel J. Microsporidia: Pathogens of Opportunity. Wiley, 2014: 203-220Crossref Scopus (44) Google Scholar,11.Dubuffet A. et al.A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems.Environ. Microbiol. 2021; 23: 4344-4359Crossref PubMed Scopus (9) Google Scholar,12.Park E. Poulin R. Revisiting the phylogeny of microsporidia.Int. J. Parasitol. 2021; 51: 855-864Crossref PubMed Scopus (9) Google Scholar,28.Wijayawardene N.N. et al.Notes for genera: basal clades of Fungi (including Aphelidiomycota, Basidiobolomycota, Chytridiomycota, Monoblepharomycota, Olpidiomycota, Rozellomycota and Zoopagomycota).Fungal Divers. 2018; 92: 43-129Crossref Scopus (62) Google Scholar, 29.Corsaro D. et al.Filling gaps in the microsporidian tree: rDNA phylogeny of Chytridiopsis typographi (Microsporidia: Chytridiopsida).Parasitol. Res. 2019; 118: 169-180Crossref PubMed Scopus (16) Google Scholar, 30.Wijayawardene N.N. Outline of Fungi and fungus-like taxa.Mycosphere. 2020; 11: 1060-1456Crossref Scopus (341) Google Scholar, 31.Trzebny A. et al.A new method of metabarcoding Microsporidia and their hosts reveals high levels of microsporidian infections in mosquitoes (Culicidae).Mol. Ecol. Resour. 2020; 20: 1486-1504Crossref PubMed Scopus (8) Google Scholar]. These studies have refined the existing clade-numbering system, providing revisions such as the subdivision of clade 4 into 4a and 4b [12.Park E. Poulin R. Revisiting the phylogeny of microsporidia.Int. J. Parasitol. 2021; 51: 855-864Crossref PubMed Scopus (9) Google Scholar]. However, despite these changes, the numbered clade system has become difficult to interpret due to changing phylogenetic tree topologies and the availability of sequenced taxa, compounded by historical inconsistencies in clade numbering (particularly regarding clades 2, 3, and 5; Figure 1). We propose the more orthodox and informative use of (informal) taxon names as the basis of microsporidian taxonomy by using order-level names for the major, strongly supported clades (Figure 1 and Table S1). Whether or not these ‘orders’ are accepted as part of the various taxonomic rankings and nomenclatural schemes currently circulating for Microsporidia is unimportant; what is important is that the group names refer to a key accepted taxonomic entity (i.e., robustly supported clade), and are therefore more informative than an abstract numbering system. The ‘orders’ we annotate onto Figure 1 are largely concordant with other circumscriptions [28.Wijayawardene N.N. et al.Notes for genera: basal clades of Fungi (including Aphelidiomycota, Basidiobolomycota, Chytridiomycota, Monoblepharomycota, Olpidiomycota, Rozellomycota and Zoopagomycota).Fungal Divers. 2018; 92: 43-129Crossref Scopus (62) Google Scholar,30.Wijayawardene N.N. Outline of Fungi and fungus-like taxa.Mycosphere. 2020; 11: 1060-1456Crossref Scopus (341) Google Scholar], except for some genera that our tree shows to have different phylogenetic affiliations.We summarise some key findings from recent microsporidian environmental sequencing studies in Figure 1 [5.Chauvet M. et al.Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem.Environ. Microbiol. 2022; 24: 1672-1686Crossref PubMed Scopus (2) Google Scholar,11.Dubuffet A. et al.A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems.Environ. Microbiol. 2021; 23: 4344-4359Crossref PubMed Scopus (9) Google Scholar,13.Ardila-Garcia A.M. et al.Microsporidian diversity in soil, sand, and compost of the Pacific Northwest.J. Eukaryot. Microbiol. 2013; 60: 601-608Crossref PubMed Scopus (17) Google Scholar,14.Williams B.A.P. et al.Group-specific environmental sequencing reveals high levels of ecological heterogeneity across the microsporidian radiation.Environ. Microbiol. Rep. 2018; 10: 328-336Crossref PubMed Scopus (23) Google Scholar]. Metabarcoding using microsporidian-specific primers on environmental samples is revealing a huge diversity of lineages, much of it related to previously characterised lineages, but also including further lineages that will both expand the size of the known subclades and result in new branches and clades being defined (Figure 1). One drawback to such data is their relatively short amplicon sequences. Robust and informative incorporation of environmentally derived sequences into SSU phylogenies ideally requires (near) full-length SSU sequences rather than short Illumina amplicons. Metabarcoding increasingly employs long-read technologies (e.g., PacBio [32.Tedersoo L. et al.PacBio metabarcoding of Fungi and other eukaryotes: errors, biases, and perspectives.New Phytol. 2018; 217: 1370-1385Crossref PubMed Scopus (142) Google Scholar] and Nanopore [33.Mafune K.K. et al.A rapid approach to profiling diverse fungal communities using the MinION™ nanopore sequencer.Biotechniques. 2020; 68: 72-78Crossref PubMed Scopus (9) Google Scholar] sequencing), which could be employed for Microsporidia using long-range SSU primers (e.g., CTMicrosp/Microsp1342r combination [34.Stentiford G.D. et al.Evidence for trophic transfer of Inodosporus octospora and Ovipleistophora arlo n. sp. (Microsporidia) between crustacean and fish hosts.Parasitology. 2018; 145: 1105-1117Crossref PubMed Scopus (22) Google Scholar]), or longer amplicons including more taxonomically informative regions (Box 1). Metabarcoding offers insight into microsporidian phylogenetics, taxonomy, and ecology, and we recommend that these data are generated and analysed in robust and consistent ways such that data from different studies are comparable.Box 1Molecular markers: a ‘minimal framework’ for microsporidian systematicsMicrosporidian taxonomy is moving towards a gold standard, which includes partial/complete genome sequencing and annotation, intracellular development and life cycle information, parasite ultrastructure, and host–parasite pathology. Strains/species can be determined without some of the above; however, we must define a minimal framework to unite ongoing efforts to catalogue microsporidian diversity, and importantly, their associated virulence and health-impacts, which inform epidemiological models and predictive emergence studies.Microsporidiologists have begun to collect sequence data for the ITS region situated between the SSU and large-subunit (LSU) ribosomal RNA genes, among other genes [68.González-Tortuero E. et al.Genetic diversity of two Daphnia-infecting microsporidian parasites, based on sequence variation in the internal transcribed spacer region.Parasit. Vectors. 2016; 9: 1-15Crossref PubMed Scopus (6) Google Scholar]. The Operophtera [69.Donahue K.L. et al.Using the SSU, ITS, and ribosomal DNA operon arrangement to characterize two Microsporidia infecting Bruce spanworm, Operophtera bruceata (Lepidoptera: Geometridae).J. Eukaryot. Microbiol. 2019; 66: 424-434Crossref PubMed Scopus (5) Google Scholar], Heterosporis [70.Tsai S.J. et al.Complete sequence and structure of ribosomal RNA gene of Heterosporis anguillarum.Dis. Aquat. Org. 2002; 49: 199-206Crossref PubMed Scopus (25) Google Scholar], Nosema [71.Hajek A.E. et al.Nosema maddoxi sp. nov. (Microsporidia, Nosematidae), a widespread pathogen of the green stink bug Chinavia hilaris (Say) and the brown marmorated stink bug Halyomorpha halys (Stål).J. Eukaryot. Microbiol. 2018; 65: 315-330Crossref PubMed Scopus (18) Google Scholar], Encephalitozoon [72.Vossbrinck C.R. et al.Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction.J. Eukaryot. Microbiol. 1993; 40: 354-362Crossref PubMed Scopus (188) Google Scholar], and Enterocytozoon [73.Li W. et al.Host specificity of Enterocytozoon bieneusi and public health implications.Trends Parasitol. 2019; 35: 436-451Abstract Full Text Full Text PDF PubMed Scopus (134) Google Scholar] have sequence data for the LSU region, used to produce more detailed phylogenetic depictions of strains and species complexes. This is especially pertinent for genera where SSU similarity is >99%, such as the Nosema, which are rooted in a deep and confusing taxonomic history [74.Tokarev Y.S. et al.A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics.J. Invertebr. Pathol. 2020; 169107279Crossref PubMed Scopus (58) Google Scholar]. For Enterocytozoon bieneusi, >1600 ITS sequences from different isolates revealed ~500 unique genotypes [73.Li W. et al.Host specificity of Enterocytozoon bieneusi and public health implications.Trends Parasitol. 2019; 35: 436-451Abstract Full Text Full Text PDF PubMed Scopus (134) Google Scholar]. Several genotypes were found only in certain hosts, suggesting strain-level host specificity [73.Li W. et al.Host specificity of Enterocytozoon bieneusi and public health implications.Trends Parasitol. 2019; 35: 436-451Abstract Full Text Full Text PDF PubMed Scopus (134) Google Scholar]. Tokarev et al. [74.Tokarev Y.S. et al.A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics.J. Invertebr. Pathol. 2020; 169107279Crossref PubMed Scopus (58) Google Scholar] showed that the RNA polymerase II gene provided additional evolutionarily distinction for Nosema. Hatjina et al. [75.Hatjina F. Polar tube protein gene diversity among Nosema ceranae strains derived from a Greek honeybee health study.J Invert. Pathol. 2011; 108: 131-134Crossref PubMed Scopus (37) Google Scholar] used the polar tube protein gene to derive Nosema strains. Bateman et al. [76.Bateman K.S. et al.Single and multi-gene phylogeny of Hepatospora (Microsporidia) – a generalist pathogen of farmed and wild crustacean hosts.Parasitology. 2016; 143: 971-982Crossref PubMed Scopus (12) Google Scholar] used the RNA polymerase, arginyl tRNA synthetase, prolyl tRNA synthetase, chitin synthase, beta tubulin, and ‘heat shock protein 70’ genes to show that Hepatospora eriocheir was a host-generalist among crab species.To achieve a minimal framework for microsporidian descriptions, we propose that ultrastructural and developmental data be collected for the parasite using transmission electron microscopy; histology (or wet-prepared tissue) to define affected organs and broader pathology; and finally, sequence the ITS region and partial/complete LSU region in addition to the SSU. The studies listed earlier provide PCR primers for some microsporidian groups, but it is acknowledged that greater long-read diversity or genome work is necessary for continued primer development (Figure I) [77.Jamy M. et al.Long-read metabarcoding of the eukaryotic rDNA operon to phylogenetically and taxonomically resolve environmental diversity.Mol. Ecol. Resour. 2020; 20: 429-443Crossref PubMed Scopus (41) Google Scholar,78.Vossbrinck C.R. et al.Ribosomal RNA sequence suggests Microsporidia are extremely ancient eukaryotes.Nature. 1987; 326: 411-414Crossref PubMed Scopus (434) Google Scholar].Figure IA MAFFT alignment of the large subunit rRNA gene of seven microsporidian species.Show full captionThe green line plot indicates regions of high and low conservation. Red broken line boxes accompanied by sequence information highlight regions where primers have been developed [72.Vossbrinck C.R. et al.Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction.J. Eukaryot. Microbiol. 1993; 40: 354-362Crossref PubMed Scopus (188) Google Scholar,78.Vossbrinck C.R. et al.Ribosomal RNA sequence suggests Microsporidia are extremely ancient eukaryotes.Nature. 1987; 326: 411-414Crossref PubMed Scopus (434) Google Scholar] (bold and underlined) as well as regions where development could be possible. The figure was designed in CLC genomics workbench v.22. See [72.Vossbrinck C.R. et al.Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction.J. Eukaryot. Microbiol. 1993; 40: 354-362Crossref PubMed Scopus (188) Google Scholar,78.Vossbrinck C.R. et al.Ribosomal RNA sequence suggests Microsporidia are extremely ancient euk" @default.
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• W4281774004 date "2022-08-01" @default.
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• W4281774004 title "Microsporidia: a new taxonomic, evolutionary, and ecological synthesis" @default.
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