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Title: Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles

Author
item Scully, Erin
item Geib, Scott
item CARLSON, JOHN - Pennsylvania State University
item TIEN, MING - Pennsylvania State University
item HOOVER, KELLI - Pennsylvania State University

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/24/2014
Publication Date: 12/12/2014
Citation: Scully, E.D., Geib, S.M., Carlson, J.E., Tien, M., Hoover, K. 2014. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. Biomed Central (BMC) Genomics 2014. 15:1096. doi:10.1186/1471-2164-15-1096.

Interpretive Summary: Wood-feeding beetles are some of the most destructive pests to forest ecosystems worldwide. We evaluated the symbiotic relationship between wood-feeding beetles and the microbes that inhabit their guts. In the Asian longhorned beetle, the gut microbial community expressed genes responsible for the synthesis of essential nutrients, whereas the insect expressed more genes involved in the digestion of woody tissue. These findings suggest that the insect and the gut microbes have separate roles but work together to meet the nutritional demands of the Asian longhorned beetle. The insect has the primary role of cellulose and plant cell wall degradation, while the gut microbes provide nutrients by converting xylose and other wood sugars into essential amino acids. This could represent an opportunity for nutrient exchange between the insect and its gut microbes where the beetle breaks down plant cell walls and releases sugars that are converted into essential nutrients by the gut microbes. These findings may provide new opportunities to control wood-feeding beetles by disrupting the gut microbes that synthesize essential nutrients for the beetle.

Technical Abstract: The gut microbial communities associated with xylophagous beetles are taxonomically rich and predominately comprised of taxa that are poised to promote survival in woody tissue, which is devoid of nitrogen and essential nutrients. However, the contributions of gut microbes to digestive physiology and nutritional ecology remain uncharacterized in many lineages and are hampered by the sizeable number of facultative symbionts. Through parallel transcriptome profiling of insect- and microbial- derived mRNAs expressed in the gut of the wood-feeding beetle Anoplophora glabripennis, we demonstrate that the microbial community has the potential to provide essential nutrients that the insect is endogenously unable to synthesize. For example, the microbial community is enriched in essential nutrient biosynthetic pathways, including essential amino acids, vitamins, and sterols, which were absent in the A. glabripennis transcriptome. Furthermore, although A. glabripennis produces a number of plant cell wall degrading enzymes, the gut microbiota produces its own suite of transcripts predicted to encode cell wall degrading enzymes. These include enzymes that can enhance lignin degradation, degrade hemicellulose, and ferment xylose and wood sugars. Transcripts providing similar functions were not expressed in A. glabripennis, suggesting that interactions with the gut community can expand A. glabripennis’ ability to digest carbohydrates and utilize wood sugars. In addition, an OTU-based metagenomic analysis was performed to determine which fraction of the microbial community is transcriptionally active. We demonstrated that OTU abundance and persistence were not necessarily correlated with transcriptional activity as a subset of both shared and rare OTUs were transcriptionally active in the midgut. This finding contradicts the common presumptions that abundance is related to ecological contribution in metagenomic studies, particularly in endosymbiont communities. This study provides new insights into nutritional provisioning capacities of microbes associated with wood-feeding insects and will ultimately permit a deeper understanding of the physiological interactions between gut symbionts and A. glabripennis.