Assembly by disassembly of the gut microbiota in Riptortus pedestris and other stinkbugs

The gut is one of the largest internal organs in animals and is central to nutrition. Its need to uptake food from the environment implies it is open at both ends, exposing its lumen to the outside world and to colonization by ingested microbial communities. As the primary site of host-associated microbiota, the gut has, over evolutionary time, fostered stable associations with specific microbes to which the host has delegated key biological functions. Insect gut microbiota is of interest both for its impact on this ecologically important animal group and as a simplified model for understanding fundamental features of host-microbiota interactions. Here, we focus on the highly distinctive midgut of phytophagous stinkbugs (Heteroptera: Pentatomomorpha) and its associated microbiota. The most distinctive feature of the midgut is a posterior crypt-bearing region that constitutes a symbiotic organ housing a single specific bacterial symbiont population. The anterior gut harbors a more diverse microbial community. In many species, like Riptortus pedestris, microbe-free newborns ingest bacteria by soil probing and gradually filter them along the anterior to posterior gut axis. The process enriches Burkholderia sensu lato until a single Caballeronia strain is established in the crypt region. We describe the selective conditions in the gut and the reciprocal symbiont traits that precisely and reproducibly shape the gut microbiota from a variable soil community. Even if the process is accurate, it is however not without vulnerabilities because it enriches Burkholderia in the gut comprising many pathogenic strains. The Caballeronia crypt symbionts and some pathogen strains can be exploited by the host to reinforce its immunity, but other strains cause deadly infections.