C-type lectin-mediated microbial homeostasis is critical for Helicoverpa armigera larval growth and development

The immune system of a host functions critically in shaping the composition of the microbiota, and some microbes are involved in regulating host endocrine system and development. However, whether the immune system acts on endocrine and development by shaping the composition of the microbiota remains unclear, and few molecular players or microbes involved in this process have been identified. In the current study, we found that RNA interference of a C-type lectin (HaCTL3) in the cotton bollworm Helicoverpa armigera suppresses ecdysone and juvenile hormone signaling, thus reducing larval body size and delaying pupation. Depletion of HaCTL3 also results in an increased abundance of Enterocuccus mundtii in the hemolymph, which may escape from the gut. Furthermore, HaCTL3 and its controlled antimicrobial peptides (attacin, lebocin, and gloverin) are involved in the clearance of E. mundtii from the hemolymph via phagocytosis or direct bactericidal activity. Injection of E. mundtii into larval hemocoel mimics HaCTL3-depleted phenotypes and suppresses ecdysone and juvenile hormone signaling. Taken together, we conclude that HaCTL3 maintains normal larval growth and development of H. armigera via suppressing the abundance of E. mundtii in the hemolymph. Our results provide the first evidence of an immune system acting on an endocrine system to modulate development via shaping the composition of microbiota in insect hemolymph. Thus, this study will deepen our understanding of the interaction between immunity and development.