Enterococcal symbionts of caterpillars facilitate the utilization of a suboptimal diet

Authors: CHEN, BOSHENG - Zhejiang A & F University; Mason, Charles; PEIFFER, MICHELLE - Pennsylvania State University; ZHANG, DAYU - Zhejiang A & F University; SHAO, YONGQI - Zhejiang A & F University; FELTON, GARY - Pennsylvania State University

Submitted to: Journal of Insect Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/8/2022
Publication Date: 2/11/2022
Citation: Chen, B., Mason, C.J., Peiffer, M., Zhang, D., Shao, Y., Felton, G.W. 2022. Enterococcal symbionts of caterpillars facilitate the utilization of a suboptimal diet. Journal of Insect Physiology. 138. Article 104369. https://doi.org/10.1016/j.jinsphys.2022.104369.
DOI: https://doi.org/10.1016/j.jinsphys.2022.104369

Interpretive Summary: Bacterial symbionts in lepidopteran insects have been suggested to impact their host through different mechanisms, but compared to other systems we lack clear experimental examples. We used fall armyworm (Spodoptera frugiperda) as a model to evaluate specific effects of gut bacteria. We generated insects that were sterile or possessed defined communities, and created sterilized artificial diets to evaluate specific effects. Following an initial screen of bacterial isolates from different genera, larvae inoculated with Enterococcus exhibited a higher body mass only when feed on pinto bean diet. Systematic screening Enterococcus isolates from fall armyworm revealed different effects on their host, where some increased larval body mass and pupal survival, while others had no effects. Reducing pinto bean diet concentration with non-nutritive cellulose revealed the presence of a potential toxin. These results indicate that some gut microorganisms of lepidopterans can benefit the host, but the dietary context is a key aspect to determine the overarching response.

Technical Abstract: Bacterial symbionts in lepidopteran insects may impact their host through different mechanisms. However, in most lepidopteran systems we lack experimental examples to explain how specific members of the gut bacterial community influence their host. We used fall armyworm (Spodoptera frugiperda) as a model system to address this core questions. In order to address the potential roles of bacteria in these systems, we implemented axenic and gnotobiotic techniques using sterile semi-artificial pinto bean (Pb) diet and a high nutrient wheat-germ (Wg) diet. Following an initial screen of bacterial isolates from different genera, larvae inoculated with Enterococcus FAW 2-1 exhibited a higher body mass only when feed on Pb diet, but not on Wg diet. Systematic screening of fall armyworm Enterococcus isolates revealed divergent effects on their host, even among phylogenetically similar isolates. Dilution of the Pb diet revealed that larvae performed better on less-concentrated diets, indicating the presence of a potential toxin. Collectively, our results demonstrate that some gut microorganisms of lepidopterans can benefit the host, but the dietary context is key towards understanding the direction of the response and magnitude of the effect. We provide an evidence that gut microorganisms may play a wider role in mediating feeding breadth lepidopteran pests, but overall impacts could be related to the environmental stress and the microorganisms inhabiting the gut.