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

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Abstract
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,ψLdcA), five rare lipoprotein As (RlpA1-5), N-acetylmuramoyl-L-alanine amidase (AmiD), 1,4-beta-N-acetylmuramidase (bLys), DNA polymerase III alpha chain (ψDnaE), and ATP synthase delta chain (ψAtpH). Buchnera was the apparent source of two highly truncated pseudogenes (ψDnaE and ψAtpH). 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 LdcAs and RlpAs 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 lineages have repeatedly evolved intimate symbioses with eukaryotic hosts, the most famous cases being those of the cell organelles, mitochondria, and plastids. Symbiont genomes typically lose many ancestral genes, raising the question of how they function with so few genes. In organelles, part of the answer involves gene transfer to the host genome, allowing maintenance of essential functions. So far, the extent of gene transfer to hosts has not been assessed for other cases of intimate, obligate symbiosis. Aphids harbor an ancient coevolved intracellular symbiont, called Buchnera. We used the newly available sequence of the pea aphid genome to conduct an exhaustive computational search for genes of bacterial ancestry. We found that no functional genes have been transferred from Buchnera, ruling out such transfer as a driving force in genome reduction in this symbiont. However, the aphid genome does contain eight transcribed genes of apparent bacterial origin, some of which have been duplicated after transfer. Based on their expression patterns, most of these appear to function specifically in the aphid-Buchnera symbiosis, presenting the possibility that the maintenance of obligate intracellular symbioses can be affected by the acquisition and duplication of genes transferred from unrelated bacterial lineages.