A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems

Dubuffet, Aurore; Chauvet, Marina; Moné, Anne; Debroas, Didier; Lepère, Cécile

doi:10.1111/1462-2920.15618

Cited by 26 publications

(77 citation statements)

References 69 publications

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“…Based on our phylogenetic analysis, freshwater Thelohania branch outside of both Clades IV and V, and importantly branch together in a well-supported group separate from the marine T. butleri (Clade V), the only ‘true’ Thelohania species with genetic data available ( Figure 6 ). Our taxonomic revision is further supported by several recent studies [ 15 , 29 ]. The sequence demarcation plot we provide illustrates the dissimilarity between marine and freshwater Thelohania , based on the SSU rRNA gene ( Figure 5 ).…”

Section: Discussionsupporting

confidence: 86%

“…Genomic data for T. contejeani also support that it is not a Clade V (Glugeida) or Thelohaniidae member [ 25 ]. Genetically, the crayfish-infecting, freshwater Thelohania currently reside within an ‘orphan’ lineage (also termed Clade VI), including Hamiltosporidium , Neoflabelliforma , and Areospora [ 26 , 27 , 28 , 29 , 30 ]. Therefore, the genetically distinct freshwater Thelohania genus requires taxonomic revision at both the genus, family, and possibly higher taxonomic levels.…”

Section: Introductionmentioning

confidence: 99%

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Revising the Freshwater Thelohania to Astathelohania gen. et comb. nov., and Description of Two New Species

et al. 2022

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Crayfish are common hosts of microsporidian parasites, prominently from the genus Thelohania. Thelohania is a polyphyletic genus, with multiple genetically distinct lineages found from freshwater and marine environments. Researchers have been calling for a revision of this group for over a decade. We provide evidence that crayfish-infecting freshwater Thelohania are genetically and phylogenetically distinct from the marine Thelohania (Clade V/Glugeida), whilst also describing two new species that give further support to the taxonomic revision. We propose that the freshwater Thelohania should be transferred to their own genus, Astathelohania gen. et comb. nov., in a new family (Astathelohaniidae n. fam.). This results in the revision of Thelohania contejeani (Astathelohania contejeani), Thelohania montirivulorum (Astathelohania montirivulorum), and Thelohania parastaci (Astathelohania parastaci). We also describe two novel muscle-infecting Astathelohania species, A. virili n. sp. and A. rusti n. sp., from North American crayfishes (Faxonius sp.). We used histological, molecular, and ultrastructural data to formally describe the novel isolates. Our data suggest that the Astathelohania are genetically distinct from other known microsporidian genera, outside any described family, and that their SSU rRNA gene sequence diversity follows their host species and native geographic location. The range of this genus currently includes North America, Europe, and Australia.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Revising the Freshwater Thelohania to Astathelohania gen. et comb. nov., and Description of Two New Species

et al. 2022

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“…The diversity of Microsporidia in lake Aydat studied here, over one year, was of the same order of magnitude with 1 472 microsporidian OTUs identified. Besides, except two clades weakly represented in the study by Dubuffet et al (2021), the same clades (I, IV1, IV2, V, VIII) were recovered. Similarly to the previous study, most of the OTUs were affiliated to clade IV2 and clade I, and most of the groups identified were also found in the study by Dubuffet et al (2021) with the exception of OTUs belonging to the Enterocytozoonidae, which appear almost only in February in our study.…”

Section: Discussionmentioning

confidence: 50%

“…Besides, except two clades weakly represented in the study by Dubuffet et al (2021), the same clades (I, IV1, IV2, V, VIII) were recovered. Similarly to the previous study, most of the OTUs were affiliated to clade IV2 and clade I, and most of the groups identified were also found in the study by Dubuffet et al (2021) with the exception of OTUs belonging to the Enterocytozoonidae, which appear almost only in February in our study. Among OTUs assigned to a genus, Crispospora and Pseudoberwaldia were the most represented.…”

Section: Discussionmentioning

confidence: 50%

Temporal variations of Microsporidia diversity and discovery of new host–parasite interactions in a lake ecosystem

Chauvet

Debroas

Moné

et al. 2022

Environmental Microbiology

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Microsporidia are a large group of obligate intracellular eukaryotic parasites related to Fungi. Recent studies suggest that their diversity has been greatly underestimated and little is known about their hosts other than metazoans, and thus about their impact on the communities at the base of the food web. In this work, we therefore studied the diversity of Microsporidia over one year and identified potential new hosts in small-sized fractions (<150 μm) in a lake ecosystem using a metabarcoding approach coupled with co-occurrence networks and tyramide signal amplification-fluorescent in situ hybridization. Our analysis shows a great Microsporidia diversity (1 472 OTUs), with an important part of this diversity being unknown. Temporal variations of this diversity have been observed, which might follow temporal variations of their potential hosts such as protists and microzooplankton. New hosts among them were identified as well as associations with phytoplankton. Indeed, repeated infections were observed in Kellicottia (rotifers) with a prevalence of 38% (infected individuals). Microsporidia inside a Stentor (ciliate) were also observed. Finally, potential infections of the diatom Asterionella were identified (prevalence <0.1%). The microsporidian host spectrum could be therefore even more important than previously described, and their role in the functioning of lake ecosystems is undoubtedly largely unknown.

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“…In addition, major advances in large-scale DNA sequencing have enabled the development of DNA metabarcoding approaches for biodiversity profiling in which different species are detected simultaneously using group-specific or universal PCR primers [ 26 , 27 ]. Such approaches have already been applied also to the detection of microsporidian biodiversity [ 28 – 30 ]. In this article, we used the DNA metabarcoding approach to examine the prevalence and diversity of microsporidians in I. ricinus to assess the role of ticks as potential vectors of microsporidian species causing diseases in humans.…”

Section: Introductionmentioning

confidence: 99%

Metabarcoding reveals low prevalence of microsporidian infections in castor bean tick (Ixodes ricinus)

et al. 2022

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Background Microsporidia is a large group of eukaryotic obligate intracellular spore-forming parasites, of which 17 species can cause microsporidiosis in humans. Most human-infecting microsporidians belong to the genera Enterocytozoon and Encephalitozoon. To date, only five microsporidian species, including Encephalitozoon-like, have been found in hard ticks (Ixodidae) using microscopic methods, but no sequence data are available for them. Furthermore, no widespread screening for microsporidian-infected ticks based on DNA analysis has been carried out to date. Thus, in this study, we applied a recently developed DNA metabarcoding method for efficient microsporidian DNA identification to assess the role of ticks as potential vectors of microsporidian species causing diseases in humans. Methods In total, 1070 (493 juvenile and 577 adult) unfed host-seeking Ixodes ricinus ticks collected at urban parks in the city of Poznan, Poland, and 94 engorged tick females fed on dogs and cats were screened for microsporidian DNA. Microsporidians were detected by PCR amplification and sequencing of the hypervariable V5 region of 18S rRNA gene (18S profiling) using the microsporidian-specific primer set. Tick species were identified morphologically and confirmed by amplification and sequencing of the shortened fragment of cytochrome c oxidase subunit I gene (mini-COI). Results All collected ticks were unambiguously assigned to I. ricinus. Potentially zoonotic Encephalitozoon intestinalis was identified in three fed ticks (3.2%) collected from three different dogs. In eight unfed host-seeking ticks (0.8%), including three males (1.1%), two females (0.7%) and three nymphs (0.7%), the new microsporidian sequence representing a species belonging to the genus Endoreticulatus was identified. Conclusions The lack of zoonotic microsporidians in host-seeking ticks suggests that I. ricinus is not involved in transmission of human-infecting microsporidians. Moreover, a very low occurrence of the other microsporidian species in both fed and host-seeking ticks implies that mechanisms exist to defend ticks against infection with these parasites. Graphical abstract

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A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems

Cited by 26 publications

References 69 publications

Revising the Freshwater Thelohania to Astathelohania gen. et comb. nov., and Description of Two New Species

Revising the Freshwater Thelohania to Astathelohania gen. et comb. nov., and Description of Two New Species

Temporal variations of Microsporidia diversity and discovery of new host–parasite interactions in a lake ecosystem

Metabarcoding reveals low prevalence of microsporidian infections in castor bean tick (Ixodes ricinus)

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