Dissecting a mutualistic interaction involving an insect-endosymbiont association

Insects and bacteria, two of the most widespread groups of organisms on earth, establish diverse symbiotic associations from strict parasitism to obligate mutualism. Mutualistic relationships can be instrumental for insects to adapt and survive, and insects are expected to have evolved ways of facilitating the colonization and proliferation of the symbiotic bacteria. Pederin-producing endosymbionts (PPE) in the rove beetle Paederus fuscipes produce the toxic substance pederin, which provides the beetle with a defense against insect and arachnid predators. Most previous studies on this mutualism have focused on the bacteria, but the molecular basis for its interactions with the beetle host are not known. Here we sequenced and annotated the genome of P. fuscipes, representing the first complete genome sequence of a member of the beetle family Staphylinidae; we found expansions of P450 and GST gene families potentially contributing to the wide distribution of P. fuscipes. By assessing the microbiota of P. fuscipes and FISH visualization, we showed that PPE were the dominant bacterial phylotype in females and were common in female reproductive organs. In addition, we found that immune genes up-regulated in reproductive tissues were hostile to Gram-positive bacteria, but likely provided a favorable environment for the colonization and proliferation of Gram-negative PPE bacteria in female reproductive tissues. This work combining multi-omics with FISH analyses thereby helps to unravel this mutualistic interaction and other mutualistic insect-endosymbiont systems.