Ophiocordyceps sinensis infection alters the immune system of the host Thitarodes xiaojinensis investigated by the interaction between immunity and gut microbiota escaping to hemolymph

Abstract

Background Ophiocordyceps sinensis as one typical entomopathogenic fungus (EPF) has the long-term symbiosis process with its host Thitarodes xiaojinensis. O. sinensismainly exists in the hemolymph of the host. However, the mechanism of the host immune response to O. sinensis remains unclear. Results Here, a multi‑omics approach was used to clarify the role of the interaction between O. sinensis and T.xiaojinensis. The infection of O. sinensis could lead to the increase of hormone levels (20-hydroxyecdysone and juvenile hormone), the enhancement of antioxidant capacity (total antioxidant capacity and glutathione S-transferase) and the response of humoral immunity based on the antibacterial peptides (AMPs) in the host T.xiaojinensis. Elevated 20E levels in the host when O. sinensis infection might contribute to the enhanced expression of AMPs. O. sinensis infection led to intestinal barrier damage and promoted the translocation of bacteria from the gut to hemocoel. Then, the presence of O. sinensis and other opportunistic pathogenic bacterium from gut disrupted the homeostasis of hemolymph microbiota and increased bacterial diversity of the hemolymph. Conclusions Overall, this study demonstrated that O. sinensis infection damaged intestinal barrier and induced the translocation of gut bacteria and the disruption of microbial homeostasis in hemolymph. The host T.xiaojinensis activated and exploited humoral antibacterial immunity and to eliminate opportunistic bacteria. our findings reveal a novel strategy of interaction between O. sinensis and T.xiaojinensis.