Shifts in Buchnera aphidicola density in soybean aphids (Aphis glycines) feeding on virus-infected soybean

Authors: CASSONE, BRYAN - The Ohio State University; Redinbaugh, Margaret; DORRANCE, ANNE - The Ohio State University; MICHEL, ANDREW - The Ohio State University

Submitted to: Insect Molecular Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/3/2015
Publication Date: 4/3/2015
Citation: Cassone, B.J., Redinbaugh, M.G., Dorrance, A.E., Michel, A.P. 2015. Shifts in Buchnera aphidicola density in soybean aphids (Aphis glycines) feeding on virus-infected soybean. Insect Molecular Biology. DOI 10.1111/imb.12170.

Interpretive Summary: Many insects carry symbiotic bacteria to help them meet their nutritional needs. These symbiotic bacteria occur in many different kinds of insects, and have played important roles in the specialization and diversification of insect species. Aphids require a symbiotic bacteria called Buchnera aphidicola to provide essential amino acids for the insect's development and reproduction. We previously found that soybean aphids feeding on plants infected with a specific virus (Bean pod mottle virus) had significantly fewer young. We thought the lower reproduction rates could be related to effects on the insect's symbiotic bacteria. We tested the abundance of bacteria in soybean aphids feeding on virus-infected and healthy plants, and determined that the population of Buchnera bacteria was dramatically reduced in aphids fed on virus-infected plants. We also determined that there were significantly lower levels of amino acid levels in leaves from virus-infected and healthy plants, suggesting that amino acids required for bacterial population growth were limiting Buchnera growth. However, we could not show that the reduced Buchnera bacteria growth caused reduced aphid reproduction, because aphids fed on soybean infected with a different virus (Soybean mosaic virus) had reduced Buchnera growth, but not reduced aphid reproduction. Our work is among the first to shoe that interactions among insects, plants, and plant pathogens influence endosymbiont populations in insects.

Technical Abstract: Bacterial symbioses are prevalent across insect taxa, and are considered key to several specialized feeding behaviors and to insect diversification at large. Aphids undergo an obligate symbiosis with Buchnera aphidicola, which provides essential amino acids to its host contributing directly to host development and fecundity. We previously found Aphis glycines feeding on BPMV-infected soybean had significantly reduced fecundity. We hypothesized that the reduction was due to detrimental impacts on the aphid microfauna, namely Buchnera. To test this hypothesis, RNA-Seq, RT-qPCR and qPCR were used to assay Buchnera transcript abundance and titer in A. glycines feeding on SMV-infected, BPMV-infected, and healthy soybean for up to 14 days. Targeted metabolite profiling was used to examine changes in amino acid content between healthy and infected soybean. Buchnera population growth was inhibited in aphids fed on either SMV- or BPMV-infected soybean, but the reduced growth was not associated with aphid fecundity. Rather, our results suggested that Buchnera population density was correlated with the amino acid content in soybean leaf extracts. Fewer Buchnera were present in insects feeding on virus-infected plants, suggesting that key amino acids nutrients needed to promote bacterial population growth limited bacterial growth. This is the first report describing how interactions among insects, plants, and plant pathogens influence endosymbiont population dynamics.