Deconstructing the integrative metabolism of psyllids and their nutritional endosymbionts using a comparative transcriptomics approach

All psyllids (Hemiptera: Psylloidea) have an obligate mutualistic relationship with the endosymbiont Candidatus Carsonella ruddii (Carsonella) for the biosynthesis of essential amino acids (EAAs) and vitamins, which are scarce in a plant sap diet. Carsonella is harbored within specialized insect cells called bacteriocytes and is metabolically integrated with its psyllid host. Carsonella retains most genes involved in the EAA biosynthetic pathways however gaps are present. It is hypothesized that psyllid host genes compensate for Carsonella’s missing genes, however, our understanding of the psyllid’s integrated metabolism is limited, and little is known about the contribution of co-nutritional endosymbionts to the EAA metabolism. To address these limitations, we analyzed gene expression profiles of the Potato psyllid Bactericera cockerelli, as well as the Asian citrus psyllid Diaphorina citri that harbors Candidatus Profftella armatura in addition to Carsonella. Our results show that bacteriocyte-specific gene expression patterns of psyllid hosts differ between host species. However, regardless of the host species, we observed significant up-regulation of the key psyllid encoded genes in the amino acid metabolism in the bacteriocyte, such as Ornithine aminotransferase (OAT) and Argininosuccinate lyase (ASL). Notably, it has been previously shown that the psyllid ASL was obtained by horizontal gene transfer from bacteria, which is an important mechanism driving coevolution between insects and their bacterial endosymbionts. We also performed comparative transcriptomic analysis to allow between-species comparisons and highlight interesting similarities and contrasts with the evolutionary history of psyllid and its endosymbionts.