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Genome reduction is typical of obligate symbionts. In cellular organelles, this reduction partly reflects transfer of ancestral bacterial genes to the host genome, but little is known about gene transfer in other obligate symbioses. Aphids harbor anciently acquired obligate mutualists,  Buchnera aphidicola  (Gammaproteobacteria), which have highly reduced genomes (420–650 kb), raising the possibility of gene transfer from ancestral  Buchnera  to the aphid genome. In addition, aphids often harbor other bacteria that also are potential sources of transferred genes. Previous limited sampling of genes expressed in bacteriocytes, the specialized cells that harbor  Buchnera , revealed that aphids acquired at least two genes from bacteria. The newly sequenced genome of the pea aphid,  Acyrthosiphon pisum , presents the first opportunity for a complete inventory of genes transferred from bacteria to the host genome in the context of an ancient obligate symbiosis. Computational screening of the entire  A. pisum  genome, followed by phylogenetic and experimental analyses, provided strong support for the transfer of 12 genes or gene fragments from bacteria to the aphid genome: three LD–carboxypeptidases ( LdcA1, LdcA2 ,ψ LdcA ), five rare lipoprotein As ( RlpA1-5 ),  N -acetylmuramoyl-L-alanine amidase ( AmiD ), 1,4-beta- N -acetylmuramidase ( bLys ), DNA polymerase III alpha chain (ψ DnaE ), and ATP synthase delta chain (ψ AtpH ).  Buchnera  was the apparent source of two highly truncated pseudogenes (ψ DnaE  and ψ AtpH ). Most other transferred genes were closely related to genes from relatives of  Wolbachia  (Alphaproteobacteria). At least eight of the transferred genes ( LdcA1 ,  AmiD ,  RlpA1-5 ,  bLys ) appear to be functional, and expression of seven ( LdcA1 ,  AmiD ,  RlpA1-5 ) are highly upregulated in bacteriocytes. The  LdcA s and  RlpA s appear to have been duplicated after transfer. Our results excluded the hypothesis that genome reduction in  Buchnera  has been accompanied by gene transfer to the host nuclear genome, but suggest that aphids utilize a set of duplicated genes acquired from other bacteria in the context of the  Buchnera –aphid mutualism.

Bacterial Genes in the Aphid Genome: Absence of Functional Gene Transfer from Buchnera to Its Host