Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont
Aphid species bear intracellular symbiotic bacteria in the cytoplasm of bacteriocytes, which are specialized cells for harboring said bacteria. This mutualism is so obligate that neither can reproduce independently. The genome sequence of the pea aphid, Acyrthosiphon pisum, in consort with that of bacterial symbiont Buchnera aphidicola illustrates the remarkable interdependency between these two organisms. The genetic capacities of the pea aphid and the symbiont for amino acid biosynthesis are complementary. Genome analysis revealed that the pea aphid has undergone characteristic gene losses and duplications. The IMB antibacterial immune pathway is missing several critical genes, which might account for the evolutionary success of aphids in obtaining beneficial symbionts. Lineage-specific gene duplications have occurred in genes over a broad range of functional categories, which include signaling pathways, miRNA machinery, chromatin modification and mitosis. The importance of these duplications for symbiosis remains to be determined. We found several instances of lateral gene transfer from bacteria to the pea aphid genome. Some of them are highly expressed in bacteriocytes.
We recently discovered a novel class of genes in the pea aphid genome that encode small cysteine-rich proteins with secretion signals that are expressed exclusively in the bacteriocytes of the pea aphid, and named these bacteriocyte-specific cysteine-rich proteins (BCR). The BCR mRNAs are first expressed at a developmental time point coinciding with the incorporation of symbionts strictly in the cells that contribute to the bacteriocyte, and this bacteriocyte-specific expression is maintained throughout the aphid’s life. Furthermore, some BCRs showed antibiotic activity. These results suggest that BCRs act within bacteriocytes to mediate the symbiosis with bacterial symbionts, which is reminiscent of the cysteine-rich secreted proteins of leguminous plants that also regulate endosymbionts. Employment of small cysteine-rich peptides may be a common tactic of host eukaryotes to manipulate bacterial symbionts.