Extended mutualism between termites and gut microbes: nutritional symbionts contribute to nest hygiene

All higher eukaryotes have established symbiotic relationships with diverse microorganisms. One of the most well-characterized symbiotic systems is that of termites and their intestinal microorganisms, which digest cellulose. Recently, diverse types of symbioses between gut microbes and host organisms including humans have received growing attention for various features of their complex interactions beyond nutrition. In termites, researchers are beginning to explore such function of gut symbionts, but only the contribution to internal immunity against entomopathogen is known in a few species. Here, we report that gut symbionts of the dampwood termite Zootermopsis nevadensis protect nests from the spread of the commensal bacterium Serratia marcescens, which has pathogenic potential. Defaunated termites dispersed S. marcescens in the surrounding environment by feeding on the bacteria, which then survived passage through their alimentary tracts, while non-defaunated termites did not. Loss of gut symbionts caused a significant reduction in intestinal acetate, which is an important carbon source for termites. Culture experiments showed that acetate had significant inhibitory effects on S. marcescens at a concentration as low as 12 mM, which indicated that the intestinal acetate of non-defaunated termites (40–130 mM) was capable of suppressing this bacterium. These results suggest that digestive derivatives produced by intestinal symbionts play an essential role in nest hygiene in addition to their nutritional function for termites. Our study provides a better understanding of the multifunctionality of symbiotic relationships in diverse organisms beyond nutrition.