Opposing growth responses of Lepidopteran larvae to the establishment of gut microbiota

Authors: Mason, Charles; PEIFFER, MICHELLE - Pennsylvania State University; CHEN, BOSHENG - Zheijiang University; HOOVER, KELLI - Pennsylvania State University; FELTON, GARY - Pennsylvania State University

Submitted to: Microbiology Spectrum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2022
Publication Date: 6/27/2022
Citation: Mason, C.J., Peiffer, M., Chen, B., Hoover, K., Felton, G.W. 2022. Opposing growth responses of Lepidopteran larvae to the establishment of gut microbiota. Microbiology Spectrum. 10(4). Article e01941-22. https://doi.org/10.1128/spectrum.01941-22.
DOI: https://doi.org/10.1128/spectrum.01941-22

Interpretive Summary: Bacteria can have diverse impacts on host performance ranging from mutualistic and parasitic attributes. This study investigated how the same gut bacteria produce positive and negative effects on caterpillar hosts, and the importance of diet and host species in mediating those directions. Enterococcus bacterial isolates were identified to substantially improve fall armyworm (Spodoptera frugiperda) performance on a suboptimal semi-artificial diet, but not on a diet that was well suited for larval rearing. When the same bacteria were provided to beet armyworm (Spodoptera exigua), we observed strong negative effects across all diets. The positive and negative effects were long-lasting, as introductions within the first 48 hours persisted for several weeks. Oral inoculations with other isolates yielded different results for both species. These results provide new understanding to how lepidopterans engage with their microbial associates and the functions in their hosts.

Technical Abstract: Gut microbiota can have diverse impacts on hosts, the nature of which often depend on the circumstances. For insect gut microbes, the quality and nature of host diets can be a significant force in swinging the pendulum from inconsequential to functionally important. In our study, we addressed whether beneficial microbes in one species impart similar functions to related species under identical conditions. Using fall armyworm (Spodoptera frugiperda), beet armyworm (Spodoptera exigua), and other noctuid hosts, we implemented an axenic rearing strategy and manipulated gut bacterial populations and dietary conditions. Our results revealed that gut some Enterococcus and Enterobacter isolates can facilitate utilization of a poor diet substrate by fall armyworm, but this was not the case for other more optimized diets. While Enterococcus provided benefits to fall armyworm, it was decidedly antagonistic to beet armyworm (Spodoptera exigua) under identical conditions. Unique isolates and bacterial introductions at early growth stages were critical to how both larval hosts performed. Our results provide robust evidence of the roles in which bacteria support lepidopteran larval growth, but also indicate that the directionality of these relationships can differ among congener hosts.