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Pea aphids (Acyrthosiphon pisum) are insects containing genes of bacterial origin with putative functions in peptidoglycan (PGN) metabolism. Of these,rlpA1-5,amiD, andldcAare highly expressed in bacteriocytes, specialized aphid cells that harbor the obligate bacterial symbiontBuchnera aphidicola, required for amino acid supplementation of the host’s nutrient-poor diet. Despite genome reduction associated with endosymbiosis, pea aphidBuchneraretains genes for the synthesis of PGN whileBuchneraof many other aphid species partially or completely lack these genes. To explore the evolution of aphid horizontally-transferred genes (HTGs) and to elucidate how host and symbiont genes contribute to PGN production, we sequenced genomes from four deeply branching lineages, such that paired aphid andBuchneragenomes are now available for 17 species representing eight subfamilies. We identified all host and symbiont genes putatively involved in PGN metabolism. Phylogenetic analyses indicate that each HTG family was present in the aphid shared ancestor, but that each underwent a unique pattern of gene loss or duplication in descendant lineages. While four aphidrlpAgene subfamilies show no relation to symbiont PGN gene repertoire, the loss of aphidamiDandldcAHTGs coincides with the loss of symbiont PGN metabolism genes. In particular, the coincident loss of hostamiDand symbiontmurCEFin tribe Aphidini, in contrast to tribe Macrosiphini, suggests either 1) functional linkage between these host and symbiont genes, or 2) Aphidini has lost functional PGN synthesis and other retained PGN pathway genes are non-functional. To test these hypotheses experimentally, we used cell-wall labeling methods involving ad-alanine probe and found that both Macrosiphini and Aphidini retainBuchneraPGN synthesis. Our results imply that compensatory adaptations can preserve PGN synthesis despite the loss of some genes considered essential for this pathway, highlighting the importance of the cell wall in these symbioses. |
