Antimicrobial Compounds in the Volatilome of Social Spider Communities

Social arthropods such as termites, ants, and bees are among others the most successful animal groups on earth. However, social arthropods face an elevated risk of infections due to the dense colony structure, which facilitates pathogen transmission. An interesting hypothesis is that social arthropods are protected by chemical compounds produced by the arthropods themselves, microbial symbionts, or plants they associate with. Stegodyphus dumicola is an African social spider species, inhabiting communal silk nests. Because of the complex three-dimensional structure of the spider nest antimicrobial volatile organic compounds (VOCs) are a promising protection against pathogens, because of their ability to diffuse through air-filled pores. We analyzed the volatilomes of S. dumicola, their nests, and capture webs in three locations in Namibia and assessed their antimicrobial potential. Volatilomes were collected using polydimethylsiloxane (PDMS) tubes and analyzed using GC/Q-TOF. We showed the presence of 199 VOCs and tentatively identified 53 VOCs. More than 40% of the tentatively identified VOCs are known for their antimicrobial activity. Here, six VOCs were confirmed by analyzing pure compounds namely acetophenone, 1,3-benzothiazole, 1-decanal, 2-decanone, 1-tetradecene, and docosane and for five of these compounds the antimicrobial activity were proven. The nest and web volatilomes had many VOCs in common, whereas the spider volatilomes were more differentiated. Clear differences were identified between the volatilomes from the different sampling sites which is likely justified by differences in the microbiomes of the spiders and nests, the plants, and the different climatic conditions. The results indicate the potential relevance of the volatilomes for the ecological success of S. dumicola.

Automated summary

Social arthropods such as termites, ants, and bees face an elevated risk of infections due to their dense colony structure, but they may be protected by chemical compounds from themselves, microbial symbionts, or associated plants. Stegodyphus dumicola, an African social spider species, may benefit from antimicrobial volatile organic compounds (VOCs) in their complex three-dimensional nests. Analysis of the volatilomes from S. dumicola in Namibia revealed potential antimicrobial activity in over 40% of identified VOCs, with certain compounds showing confirmed antimicrobial properties. Differences in volatilome composition between spiders, nests, and webs from different locations suggest a potential role in ecological success for S. dumicola.