Specific Midgut Region Controlling the Symbiont Population in an Insect-Microbe Gut Symbiotic Association

Abstract

ABSTRACTMany insects possess symbiotic bacteria that affect the biology of the host. The level of the symbiont population in the host is a pivotal factor that modulates the biological outcome of the symbiotic association. Hence, the symbiont population should be maintained at a proper level by the host's control mechanisms. Several mechanisms for controlling intracellular symbionts of insects have been reported, while mechanisms for controlling extracellular gut symbionts of insects are poorly understood. The bean bugRiptortus pedestrisharbors a betaproteobacterial extracellular symbiont of the genusBurkholderiain the midgut symbiotic organ designated the M4 region. We found that the M4B region, which is directly connected to the M4 region, also harborsBurkholderiasymbiont cells, but the symbionts therein are mostly dead. A series of experiments demonstrated that the M4B region exhibits antimicrobial activity, and the antimicrobial activity is specifically potent against theBurkholderiasymbiont but not the culturedBurkholderiaand other bacteria. The antimicrobial activity of the M4B region was detected in symbiotic host insects, reaching its highest point at the fifth instar, but not in aposymbiotic host insects, which suggests the possibility of symbiont-mediated induction of the antimicrobial activity. This antimicrobial activity was not associated with upregulation of antimicrobial peptides of the host. Based on these results, we propose that the M4B region is a specialized gut region ofR. pedestristhat plays a critical role in controlling the population of theBurkholderiagut symbiont. The molecular basis of the antimicrobial activity is of great interest and deserves future study.