This study provides a comprehensive taxonomic description of a microsporidian parasite infecting crickets, Gryllus bimaculatus and G. assimilis. Our analysis includes gross pathology, histopathology, spore ultrastructure, parasite development cycle, single gene phylogenies, and phylogenomic comparisons. We introduce a new taxon, Albopleistophora grylli n. gen. n. sp., characterised by its unique developmental stages within a sporophorous vesicle, leading to the formation of mature spores measuring 5.7 × 2.8 µm. Although prevalent in commercial cricket cultures, this parasite seemed to have limited effects on cricket survival. Indeed, microsporidia exposure and density assays with the host G. bimaculatus, only revealed density as a significant factor affecting the crickets’ survival. Nevertheless, exposure showed significant effect on the crickets’ emergence time, where exposed crickets emerged as adults earlier than unexposed individuals. Moreover, exposure to the parasite increased the faeces production and weight gain in cricket males. However, neither exposure nor density significantly impacted the females’ fecundity. The absence of spores in non-exposed cricket groups suggested a horizontal transmission, highlighting the importance of controlled rearing practices to eliminate this microsporidium in control groups. The well-known anti-microsporidian drug ‘fumagillin’ was studied with a higher microsporidia dose of exposure to evaluate any improvement in cricket survival, without showing any significant differences between exposed and unexposed groups. Our findings underscore the nuanced dynamics of host-microsporidia interactions and emphasise the need for ecological context in understanding microsporidian impacts. Even if non-dangerous for its host, monitoring of this parasite seems crucial due to its potential zoonotic transmission by its close phylogenomic relation to human-infecting microsporidia species.
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