Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis)

Authors: Scully, Erin; Geib, Scott; MASON, CHARLES - Pennsylvania State University; CARLSON, JOHN - Pennsylvania State University; TIEN, MING - Pennsylvania State University; CHEN, HAN-YI - North Carolina State University; HARDING, SCOTT - University Of Georgia; TSAI, CHUNG-JUI - University Of Georgia; HOOVER, KELLI - Pennsylvania State University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/29/2018
Publication Date: 6/25/2018
Publication URL: https://handle.nal.usda.gov/10113/6743194
Citation: Scully, E.D., Geib, S.M., Mason, C.J., Carlson, J.E., Tien, M., Chen, H., Harding, S., Tsai, C., Hoover, K. 2018. Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis). Scientific Reports. 8:9620. doi:10.1038/s41598-018-27476-0.
DOI: https://doi.org/10.1038/s41598-018-27476-0

Interpretive Summary: The Asian longhorned beetle (ALB; Anoplophora glabripennis) is an invasive, wood-boring beetle capable of feeding on over 100 broadleaf tree species that has established itself in the Northeastern and Midwestern United States. Due to its broad host range, this insect is considered one of the biggest threats to forest ecosystems and urban landscapes in the world. This insect copes with the challenges of feeding on multiple tree species through its collaboration with microbial partners in the gut that aid in the digestion of plant material, acquisition of essential nutrients, and detoxification of toxins produced by plants that can have negative impacts on fitness. Additionally, the beetle itself produces an impressive arsenal of digestive and detoxification enzymes whose activity levels can be fine-tuned to enable the insect to thrive while feeding on such a broad range of plants. Despite ALB’s broad host range, several tree species have resistance, including Chinese white poplar (Populus tomentosa). This tree species produces higher levels of two defensive compounds (salicin and tremulacin) relative to black poplar (Populus nigra), a susceptible host, that may have negative impacts on ALB fitness and deter feeding. In addition, feeding on P. tomentosa significantly reduced insect growth rate in comparison to insects reared on P. nigra, reduced the number of bacterial gut community members, and reduced the expression of several genes that produce detoxification enzymes. The identification of plant defensive compounds that negatively impact ALB fitness by disrupting interactions with beneficial bacteria or reducing the expression levels of genes linked to detoxification could lead to improved control methods.

Technical Abstract: Polyphagous insect herbivores have multiple mechanisms in place to overcome the dietary challenges of feeding in multiple plant species including, but not limited to, transcriptional plasticity and associations with obligate or facultative symbionts. The Asian longhorned beetle (Anoplophora glabripennis) is a polyphagous wood-feeder capable of developing on over 100 broadleaf tree species and, like other polyphages, its genome contains amplifications of digestive and detoxification genes. Its gut microbial community also has the metabolic potential to augment this insect’s detoxification and digestive capabilities. While the genomic repertoires of A. glabripennis and its microbial community have been studied previously, comparatively less is known about how the gut transcriptome and gut community changes in response to feeding in different hosts. In this study, we show that feeding in two suitable hosts (Acer spp. and Populus nigra) alters the expression levels of multicopy genes linked to digestion and detoxification; however, feeding in a resistant host (Populus tomentosa) induces changes in the transcriptome and gut community beyond what was observed in insects reared in P. nigra, including the downregulation of numerous ß-glucosidases, the upregulation of several cuticular genes, and the reduction of bacterial community richness by 50%. These changes may be linked to the higher constitutive levels of salicin and tremulacin produced by P. tomentosa.