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• A microsporidium Jirovecia sinensis sp. n. is described from an oligochaete. • Phylogenetic analyses positions J. sinensis in the Bacillidium - Janacekia - Pseudonosema clade. • The first SSU rDNA sequence of a species in Genus Jirovecia is provided. • Pinocytotic canals were located in the periphery of infected coelomocytes. • The pinocytotic canals may be related to nutrient acquisition from the host. We report a new microsporidium Jirovecia sinensis sp. n. from a freshwater oligochaete, Branchiura sowerbyi collected in Hongze city, Jiangsu province, East China. Numerous whitish hypertrophied coelomocytes of 0.33–0.59 mm in diameter indicated infection. Transmission electron microscopy observations revealed that all developmental stages were diplokaryotic. The earliest life stages observed were meronts that were in direct contact with host cytoplasm, accumulated peripherally in the hypertrophied coelomocytes and connected with host cytoplasm through many pinocytotic canals. Mature spores are rod-shaped with a blunt end, measuring 17.0 ± 0.1 (14.9–18.5) μm long and 2.0 ± 0.2 (1.7–2.2) μm wide. The most conspicuous character of the novel microsporidian parasite is the tail-like posterior prolongations, with a length of 29.6–40.8 μm. Mature spores have a manubrium with a diameter of 447–485 nm which consist of six density-discontinuous concentric circles. Spores possess a collar-shaped anchoring disk and a bipartite polarplast with an anterior lamellar region and a posterior tubular section. SSU rDNA-based phylogenetic analysis indicated with high support values that the new species clustered with two Bacillidium species (B. vesiculoformis and Bacillidium sp.) infecting the freshwater oligochaetes and Janacekia debaisieuxi infecting the insect Simulium maculatum. Based on the ultrastructural features and molecular characteristics, a new species in the genus Jirovecia , Jirovecia sinensis sp. n., is designated. [ABSTRACT FROM AUTHOR]