Host resistance to bacillus thuringiensis is linked to altered bacterial community within a specialist insect herbivore

Authors: PADDOCK, KYLE - University Of Missouri; PEREIRA, ADRIANO - University Of Missouri; FINKE, DEBORAH - University Of Missouri; ERICSSON, AARON - University Of Missouri; Hibbard, Bruce; Shelby, Kent

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2021
Publication Date: 11/9/2021
Citation: Paddock, K.J., Pereira, A.E., Finke, D.L., Ericsson, A.C., Hibbard, B.E., Shelby, K. 2021. Host resistance to bacillus thuringiensis is linked to altered bacterial community within a specialist insect herbivore. Molecular Ecology. 30(21):5438-5453. https://doi.org/10.1111/mec.15875.
DOI: https://doi.org/10.1111/mec.15875

Interpretive Summary: Corn rootworms are rapidly developing resistance in the field to transgenic corn expressing rootworm-specific toxins. This threatens one of the few remaining management options that Corn Belt growers have for controlling this root chewing pest. The toxins kill corn rootworm larvae by damaging their intestinal lining, allowing microbes to leak from the intestine into the blood, causing a fatal infection. Therefore the types of microbes present or missing within the rootworms could determine their sensitivity to poisons. In our study, we characterized the associated bacteria of toxin-resistant and toxin-susceptible western corn rootworm larvae. We found that resistant larvae harbored fewer bacteria and were distinct from those of susceptible larvae. Feeding on toxin-expressing maize by susceptible insects caused major changes in bacteria present, whereas the bacteria within resistant insects remained relatively unchanged. These results demonstrate that resistance to toxins is associated bacterial alterations. Our work suggests that corn rootworm microbes could be manipulated by seed coatings, soil amendments or producer actions to limit development of resistance, or even to hasten death thereby limiting chewing damage to corn roots.

Technical Abstract: Evolution of resistance to transgenic crops producing toxins from Bacillus thuringiensis (Bt) threatens the sustainability of the technology. Examination of resistance mechanisms has largely focused on characterization of mutations in proteins serving as Bt toxin binding sites. However, insect microbial communities have the potential to provide host resistance to pesticides in a myriad of ways. Previous findings suggest the killing mechanism of Bt relies on enteric bacteria becoming pathogenic in the disrupted gut environment of the insect following Bt intoxication. Thus, here we hypothesized that resistance to Bt would alter the microbiome composition of the insect. Previous studies have manipulated the microbiome of susceptible insects and monitored their response to Bt. In our study, we characterized the associated bacterial communities of Bt-resistant and -susceptible western corn rootworms, a widespread pest of maize in the United States. We found resistant insects harbor a bacterial community that is less rich and distinct from susceptible insects. After feeding on Bt-expressing maize, susceptible insects exhibited dysbiosis of the associated bacterial community, whereas the community within resistant insects remained relatively unchanged. These results suggest resistance to Bt produces alterations in the microbiome of the western corn rootworm that may contribute to resistance. We further demonstrated that by itself, feeding on Bt toxin-expressing seedlings caused a shift in the microbiota. This work provides a broader picture of the effect stressors have on microbiome composition, and the potential heritable changes induced as a result of intense selection.