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The fungus  Nosema bombycis  causes significant economic losses via parasitism of an economically important insect. MicroRNAs (miRNAs) play important roles in regulating host and parasite gene expression via mRNA degradation or by inhibiting protein translation. To investigate whether microRNA-like RNAs (milRNAs) regulate  N. bombycis  pathogenesis and to better understand the regulatory mechanisms underlying infection, we constructed small RNA libraries from  N. bombycis  hyphae during the schizont proliferation period. Eleven novel milRNAs were determined by RNA sequencing and stem-loop reverse transcriptase PCR (RT-PCR) assays. Moreover, a virulence-associated milRNA, Nb-milR8, was identified as critical for  N. bombycis  proliferation by binding and downregulating expression of its target gene,  BmPEX16 , in the host during infection. Silencing of Nb-milR8 or overexpression of the target  BmPEX16  gene resulted in increased susceptibility of  Bombyx mori  to  N. bombycis  infection. Taken together, these results suggest that Nb-milR8 is an important virulence factor that acts as an effector to suppress host peroxidase metabolism, thereby facilitating  N. bombycis  proliferation. These results provide important novel insights into interactions between pathogenic fungi and their hosts.   IMPORTANCE  A thorough understanding of fungal pathogen adaptations is essential for treating fungal infections. Recent studies have suggested that the role of small RNAs expressed in fungal microsporidia genomes are important for elucidating the mechanisms of fungal infections. Here, we report 11 novel microRNA-like RNAs (milRNAs) from the fungal microsporidium  Nosema bombycis  and identified NB-milRNAs that adaptively regulate  N. bombycis  proliferation. In addition, we demonstrate that  N. bombycis  modulates small RNA (sRNA)-mediated infection by encoding an Nb-miR8 that downregulates the expression of the host peroxidase metabolism protein BmPEX16, which is essential for peroxisome membrane biogenesis and peroxisome assembly. These results significantly contribute to our understanding of the pathogenic mechanisms of fungi, and especially microsporidia, while providing important targets for genetical engineering-based treatment of microsporidia.

Nosema bombycis microRNA-like RNA 8 (Nb-milR8) Increases Fungal Pathogenicity by Modulating BmPEX16 Gene Expression in Its Host, Bombyx mori