PGRP-S1 Maintains Gut Microbiota Homeostasis of a Notorious Insect Pest by Negatively Regulating Intestine Immunity

Red palm weevil (RPW) Rhynchophorus ferrugineus Olivier is a non-native stem-boring pest in China that has established symbiotic interactions with gut microbiota. However, the molecular mechanisms by which RPW avoids aberrant immune activation to maintain gut microbiota homeostasis remain poorly understood. Here, we found that RfPGRP-S1 is a secreted peptidoglycan recognition protein (PGRP) with amidase activity, and it is present in the gut with the highest expression level. Furthermore, RfPGRP-S1 could be drastically induced to be expressed upon bacterial challenge. rRfPGRP-S1 caused significant bacterial agglutination and significantly retarded the growth of S. aureus. RfPGRP-S1 knockdown dramatically decreased the persistence of introduced E. coli in the gut and hemolymph and the load of the indigenous gut microbiota, with intensively altered bacterial compositions. However, higher expression levels of RfDefensin were detected in the gut after RfPGRP-S1 silencing. Collectively, we found that RfPGRP-S1 maintains gut bacterial homeostasis by preventing the excessive activation of intestinal immunity via its amidase activity.