Microsporidia: a new taxonomic, evolutionary, and ecological synthesis

Bojko, Jamie; Reinke, Aaron W.; Stentiford, Grant D.; Williams, Bryony A. P.; Rogers, Martin S. J.; Bass, David

doi:10.1016/j.pt.2022.05.007

“…Microsporidia are obligate eukaryotic intracellular pathogens [ 1 ]. This fungal-related phylum contains over 1400 described species that infect a wide range of animal hosts including invertebrates, vertebrates, and protists [ 2 , 3 ]. Although as a phylum microsporidia infect a wide range of hosts, most species only infect one or several closely related hosts [ 4 , 5 ].…”

Section: Introductionmentioning

confidence: 99%

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

Wan

¹

,

Troemel

²

,

Reinke

³

2022

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Microsporidia are obligate intracellular parasites that are known to infect most types of animals. Many species of microsporidia can infect multiple related hosts, but it is not known if microsporidia express different genes depending upon which host species is infected or if the host response to infection is specific to each microsporidia species. To address these questions, we took advantage of two species of Nematocida microsporidia, N. parisii and N. ausubeli, that infect two species of Caenorhabditis nematodes, C. elegans and C. briggsae. We performed RNA-seq at several time points for each host infected with either microsporidia species. We observed that Nematocida transcription was largely independent of its host. We also observed that the host transcriptional response was similar when infected with either microsporidia species. Finally, we analyzed if the host response to microsporidia infection was conserved across host species. We observed that although many of the genes upregulated in response to infection are not direct orthologs, the same expanded gene families are upregulated in both Caenorhabditis hosts. Together our results describe the transcriptional interactions of Nematocida infection in Caenorhabditis hosts and demonstrate that these responses are evolutionarily conserved.

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“…Microsporidia are obligate eukaryotic intracellular pathogens (Vávra and Lukeš, 2013). This fungal-related phylum contains over 1400 described species that infect a wide range of animal hosts including invertebrates, vertebrates, and protists (Stentiford et al ., 2016; Bojko et al ., 2022). Although as a phylum microsporidia infect a wide range of hosts, most species only infect one or several closely related hosts (Murareanu et al ., 2021; Willis and Reinke, 2022).…”

Section: Introductionmentioning

confidence: 99%

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

Wan

¹

,

Troemel

²

,

Reinke

³

2022

Preprint

Self Cite

1

0

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Microsporidia are obligate intracellular parasites that are known to infect most types of animals. Many species of microsporidia can infect multiple related hosts, but it is not known if microsporidia express different genes depending upon which host species is infected or if the host response to infection is specific to each microsporidia species. To address these questions, we took advantage of two species of Nematocida microsporidia, N. parisii and N. ausubeli, that infect two species of Caenorhabditis nematodes, C. elegans and C. briggsae. We performed RNA-seq at several time points for each host infected with either microsporidia species. We observed that Nematocida transcription was largely independent of its host. We also observed that the host transcriptional response was similar when infected with either microsporidia species. Finally, we analyzed if the host response to microsporidia infection was conserved across host species. We observed that although many of the genes upregulated in response to infection are not direct orthologs, the same expanded gene families are upregulated in both Caenorhabditis hosts. Together our results describe the transcriptional interactions of Nematocida infection in Caenorhabditis hosts and demonstrate that these responses are evolutionarily conserved.Significance statementMicrosporidia are a powerful model to study pathogen evolution, but much is still unknown about how these pathogens have evolved to infect multiple host species. We found that microsporidia express most of their genes similarly even when they are infecting different host species and that related host species respond similarly to different microsporidia. Our results suggests that there are conserved transcriptional responses during microsporidia infection.

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“…In addition to being infected by N. parisii, C. elegans is also infected by Pancytospora epiphaga. This species infects the epidermis of C. elegans and belongs to the Enterocytozoonida clade which includes the human infecting species Vittaformae cornea and Enterocytozoon bieneusi (22, 51). To determine if dexrazoxane could inhibit P. epiphaga proliferation, we infected C. elegans with this species and monitored parasite growth using FISH staining (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Anncaliia algerae infects both mosquitos and humans and belongs to the Neopereziida clade of microsporidia (51, 52). To test whether dexrazoxane could also prevent inhibition of this species, we infected human fibroblast cells with A. algerae and visualized infection using FISH (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Encephalitozoon intestinalis infects humans and other mammals and belongs to the Nosematida clade of microsporidia (51, 53). To determine if the compounds we identified could block spore firing in this species we pre-treated E. intestinalis spores with menadione, plumbagin, thymoquinone, or ZPCK, and then carried out an in vitro spore germination assay, in which we can directly observe polar tube firing.…”

Section: Resultsmentioning

confidence: 99%

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High-throughput small molecule screen identifies inhibitors of microsporidia invasion and proliferation in C. elegans

Murareanu

¹

,

Knox

²

,

Roy

³

et al. 2021

Preprint

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Microsporidia are a diverse group of fungal-related obligate intracellular parasites that infect most animal phyla. Despite the emerging threat that microsporidia have become to humans and agricultural animals, few reliable treatment options exist. To identify novel chemical inhibitors of microsporidia infection, we developed a high-throughput screening method using Caenorhabditis elegans and the microsporidia species Nematocida parisii. We screened the Spectrum Collection of 2,560 FDA-approved compounds and natural products to identify compounds that prevent C. elegans progeny inhibition caused by N. parisii infection. We developed a semi-automated method for quantifying C. elegans progeny number in liquid culture, confirming 11 candidate microsporidia inhibitors. We show that five compounds prevent microsporidia infection by inhibiting spore firing, and demonstrate that one compound, dexrazoxane, slows infection progression. Together, our results demonstrate the effectiveness of C. elegans as a model host for drug discovery against intracellular pathogens and provide a scalable high-throughput system for the identification and characterization of additional microsporidia inhibitors.

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Microsporidia: a new taxonomic, evolutionary, and ecological synthesis

Cited by 82 publications

References 85 publications

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

Conservation of Nematocida microsporidia gene expression and host response in Caenorhabditis nematodes

High-throughput small molecule screen identifies inhibitors of microsporidia invasion and proliferation in C. elegans

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