Host and microbial defenses against fungal invaders in a fungus-farming termite

Abstract

Fungus farming in termites is vulnerable to invasions by opportunistic and specialized fungi that may compromise the Termitomyces fungal crop that these termites rely on for food. Both termite and symbiont defenses contribute to suppressing such fungal infections, and here we build on past efforts to help understand these defenses. We demonstrate that gardens without Macrotermes annandalei termites are rapidly colonized by weedy fungi, initially dominated by opportunistic Aspergillus and Trichoderma molds and later by co-evolved Xylaria that outcompete these molds. In some cases, termite presence suppresses molds but not Xylaria infections. We then demonstrate that termite burying behavior, a defense response to weeds, increases in the presence of Termitomyces, suggesting that the perception of weeds as threats is most pronounced when there is a risk of garden exposure. The burying response was strongest toward Aspergillus and Trichoderma, suggesting that coevolved Xylaria may to some extent evade this defense. Lastly, we document antifungal properties of Bacillus and Burkholderia bacteria, and 21 fungi isolated from the symbiotic environment, in support that both hosts and fungistatic microbes contribute to keeping fungal gardens free from unwanted fungi. Although our findings suggest a multi-partnered defense, further work is needed to determine the compounds responsible and their ecological significance in protecting termite gardens.