Unveiling the conserved mechanism of microsporidian vertical transmission: A comparative study of <i>Nosema</i> infection across host species

Microsporidia, ubiquitous obligate intracellular parasites infecting a wide range of hosts from humans to economically vital animals, employ transovarial transmission (TOT) as their primary vertical transmission mode. Despite its significance, the mechanisms underpinning microsporidian TOT have remained elusive. This study comparatively analyzed the TOT in two distinct systems: <i>Nosema pernyi</i> infecting wild tussah <i>Antheraea pernyi</i>, and <i>Nosema bombycis</i> infecting domestic silkworms <i>Bombyx mori</i> and crop pests <i>Spodoptera litura</i> and <i>Helicoverpa armigera</i>. Our findings reveal that both parasites share a conserved invasion sequence targeting ovariole sheath cells, follicular cells, nurse cells, and ultimately oocytes. Notably, infection of follicular and nurse cells consistently precedes oocyte invasion, suggesting a strategic utilization of these cells for efficient transmission. Contrasting patterns were observed between the two parasites: while <i>N. bombycis</i> exhibits lower infection rates and produces mature spores in both oocytes and nurse cells, <i>N. pernyi</i> displays higher parasite loads with proliferative stages predominant throughout infection. A critical innovation emerges from our RNA interference experiments, where knockdown of host vitellogenin (Vg) significantly reduced microsporidian loads, identifying Vg as a conserved molecular facilitator in TOT. These findings not only elucidate the evolutionary conservation of vertical transmission mechanisms among microsporidia but also pinpoint Vg as a promising target for intervention against these pathogens. This research advances our understanding of vertical transmission of fungal parasites and offers novel avenues for disease control.