The First Report on the Transovarial Transmission of Microsporidian Nosema bombycis in Lepidopteran Crop Pests Spodoptera litura and Helicoverpa armigera

Abstract

Microsporidia are ubiquitous fungi-related parasites infecting nearly all vertebrates and invertebrates. Microsporidian <i>Nosema bombycis</i> is a natural pathogen of multiple insects, including the silkworm and many agricultural and forest pests. <i>N. bombycis</i> can transovarially transmit in silkworm and cause huge economic losses to the sericulture. However, it remains unclear whether <i>N. bombycis</i> vertically transmits in the crop pests <i>Spodoptera litura</i> and <i>Helicoverpa armigera</i>. Here, we investigated the infection of <i>N. bombycis</i> in <i>S. litura</i> and <i>H. armigera</i> to illuminate its infectivity and transovarial transmission. In result, tissue examination with light microscopy revealed that the fat body, midgut, malpighian tubules, hemolymph, testis, and ovary were all infected in both pest pupae. Immunohistochemical analysis (IHA) of the ovariole showed that a large number of parasites in maturation and proliferation presented in follicle cell, nurse cell, and oocyte, suggesting that <i>N. bombycis</i> can infect and multiply in these cells and probably transovarially transmit to the next generations in both pests. Microscopic examination on the egg infection rate demonstrated that 50% and 38% of the <i>S. litura</i> and <i>H. armigera</i> eggs were congenitally infected, respectively. IHA of both eggs manifested numerous spores and proliferative pathogens in the oocyte, confirming that <i>N. bombycis</i> can invade into the female germ cell from the parent body. After hatching of the infected eggs, we detected the infection in offspring larvae and found large quantities of proliferative pathogens, confirming that <i>N. bombycis</i> can transovarially transmit in <i>S. litura</i> and <i>H. armigera</i>, and probably persists in both pest populations via congenital infection. In summary, our work, for the first time, proved that <i>N. bombycis</i> is able to vertically transmit in <i>S. litura</i> and <i>H. armigera</i> via infecting the oocyte in the parent, suggesting that <i>N. bombycis</i> could be a biological insecticide for controlling the population of crop pests.