Gut bacteria mediate aggregation in the German cockroach

Authors: WADA-KATSUMATA, AYAKO - North Carolina State University; ZUREK, LUDEK - Kansas State University; NALYANYA, GODFREY - North Carolina State University; ROELOFS, WENDELL - New York State Agriculture Experiment Station; Zhang, Aijun; SCHAL, COBY - North Carolina State University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/2/2015
Publication Date: 12/22/2015
Citation: Wada-Katsumata, A., Zurek, L., Nalyanya, G., Roelofs, W.L., Zhang, A., Schal, C. 2015. Gut bacteria mediate aggregation in the German cockroach. Proceedings of the National Academy of Sciences. 112(51):15678-15683.

Interpretive Summary: Cockroaches are well known to regularly move between sewers and human food materials. They have long been recognized as pests of economic and aesthetic concern and have become increasingly important in public health and veterinary medicine. The German cockroach occurs widely in buildings, and is particularly associated with restaurants, food processing facilities, hotels, and institutional establishments such as nursing homes, where it can acquire and transmit pathogens, contaminate food, cause allergic disease and serve as a mechanical vector of pathogens. It has become one of the most important residential and food-associated pests worldwide. Suppression of cockroach populations has resulted in the use of large amounts of pesticides. Application of broad spectrum toxins is a serious environmental risk and can foster insecticide resistance and make subsequent insect control more difficult. Therefore, there is an urgent need for the development of effective, safe, and environmentally compatible insect control techniques. In recent years, insect-produced volatile attractants have been recognized as useful component in successful pest control program. Although female-produced sex attractants of German cockroach have been identified, they only attract males. The aggregation attractant has been paid more attention because it can attract both sexes, making it more efficient in insect control program. Because feces-associated compounds of German cockroach have functioned as powerful attractants and arrestants in all life stages, more than 150 compounds including 57 carboxylic acids (CAs) have been identified from feces of the German cockroach. But, only a mix of 6 CAs was considered the likely aggregation agents. In this study, we have demonstrated that the gut bacteria impact the production of fecal CAs as aggregation agents and discovered that a synthetic blend of CAs was an effective aggregation stimulus for German cockroaches. Aggregation stimuli might provide the German cockroach explicit information about the physiological status of the colony (health, infections, demography) and environmental conditions such as population density. This research result enables scientists to develop a new and much more efficient tool in cockroach population detection, monitoring, and control for worldwide consumers.

Technical Abstract: Aggregation of the German cockroach, Blattella germanica, is regulated by fecal aggregation agents (pheromones), including volatile carboxylic acids (VCAs). We hypothesized that the gut microbial community contributes to production of these semiochemicals. Chemical analysis of the fecal extract of B. germanica revealed 40 VCAs. Feces from axenic cockroaches (no microorganisms in the alimentary tract) lacked 12 major fecal VCAs and 24 of the remaining compounds were represented at extremely low amounts. Olfactory and aggregation bioassays demonstrated that nymphs strongly preferred the control feces extract over the fecal extract of axenic cockroaches. Additionally, nymphs preferred a synthetic blend of six fecal VCAs over a solvent control or a previously identified VCA blend. To test whether gut bacteria contribute to the production of fecal aggregation agents, fecal aerobic bacteria were cultured, isolated, and identified. Inoculation of axenic cockroaches with individual bacterial taxa significantly rescued the aggregation response to the fecal extract, and inoculation with a mix of six bacteria isolates was more effective than with single isolates. The results demonstrate that the commensal gut microbiota contributes to production of VCAs that act as fecal aggregation agents, and that cockroaches prefer the complex odors that emanate from a diverse microbial community. We suggest that cockroach aggregation ‘pheromones’ reflect the microbial community of their local environment, possibly explaining why different compounds have been proposed as aggregation pheromones. Moreover, cockroaches may use fecal VCAs of microbial origin as chemical signatures of their colony-specific odor, enabling fidelity to persistent aggregation sites.