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 Nosema bombycis is a natural pathogen of multiple insects, including the silkworm and many agricultural and forest pests. N. bombycis can transovarially transmit in silkworm and cause huge economic losses to the sericulture. However, it remains unclear whether N. bombycis vertically transmits in the crop pests Spodoptera litura and Helicoverpa armigera. Here, we investigated the infection of N. bombycis in S. litura and H. armigera 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 N. bombycis 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 S. litura and H. armigera eggs were congenitally infected, respectively. IHA of both eggs manifested numerous spores and proliferative pathogens in the oocyte, confirming that N. bombycis 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 N. bombycis can transovarially transmit in S. litura and H. armigera, and probably persists in both pest populations via congenital infection. In summary, our work, for the first time, proved that N. bombycis is able to vertically transmit in S. litura and H. armigera via infecting the oocyte in the parent, suggesting that N. bombycis could be a biological insecticide for controlling the population of crop pests.

New insights into the genome and transmission of the microsporidian pathogen Nosema muscidifuracis

“…Staining with the DNA intercalating agent DAPI revealed puncta of ~2 μM in diameter, much smaller than nurse cell or follicle cell nuclei, in ovarioles from M. zaraptor and M. raptor but not M. uniraptor. These puncta, which are consistent in appearance with previous observations of N. muscidifuracis (Pei et al, 2021), are associated with developing egg chambers at all stages and can be readily distinguished inside latestage oocytes (Figure 6). Infected ovarioles also demonstrate signs of infection in other cell types, including nurse cells and follicle epithelial cells (Figure 6).…”

“…Transovarial transmission of unicellular parasites has been observed and reported in microsporidia ( Becnel, 1994 ; Terry et al, 1997 ; Dunn et al, 2001 ; Pei et al, 2021 ). In this study, we established vertical transmission of N. muscidifuracis in the parasitoid wasps Muscidifurax zaraptor and M. raptor through straining experiments in the ovaries of infected females.…”

Sources of Fungal Symbionts in the Microbiome of a Mobile Insect Host, Spodoptera frugiperda

“…Although our understanding of vertical transmission from parent to offspring among insects has been primarily derived from studies of bacterial symbionts [57][58][59][60][61], vertical transmission of fungal symbionts in insects does occur [56,[62][63][64]. Transovarial transmission was recently demonstrated as a mechanism for Ophiocordyceps fungal symbionts of scale insects [63], as well as for the microsporidian pathogen Nosema bombycis in the related tobacco cutworm pest Spodoptera litura [65]. Although S. frugiperda may harbor a few taxa that are vertically transmitted, perhaps those we identify as core, and shared across a majority of insects sampled (Table S1), we infer that the strong source contribution of conspecific insects found by FEAST is more likely due to horizontal transmission, the acquisition of microbial symbionts from other insects or from shared environmental sources.…”

Heterologous Expressed NbSWP12 from Microsporidia Nosema bombycis Can Bind with Phosphatidylinositol 3-Phosphate and Affect Vesicle Genesis

“…To achieve their proliferation and development, transporters or endocytosis are used by microsporidia to steal energy and metabolites from host cells [ 1 , 4 ]. Nosema bombycis , the earliest named microsporidium, is the pathogen of the silkworm Bombyx mori and has been isolated from several lepidoptera [ 5 , 6 ]. Several key genes of the vesicle transport pathway have been identified in the genome of N. bombycis [ 7 ].…”