Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host

PLoS Genet. 2010 Feb 26;6(2):e1000827. doi: 10.1371/journal.pgen.1000827.

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,psiLdcA), five rare lipoprotein As (RlpA1-5), N-acetylmuramoyl-L-alanine amidase (AmiD), 1,4-beta-N-acetylmuramidase (bLys), DNA polymerase III alpha chain (psiDnaE), and ATP synthase delta chain (psiAtpH). Buchnera was the apparent source of two highly truncated pseudogenes (psiDnaE and psiAtpH). 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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Aphids / genetics*
  • Aphids / microbiology*
  • Bacterial Proteins / genetics
  • Buchnera / enzymology
  • Buchnera / genetics*
  • Carboxypeptidases / genetics
  • DNA Polymerase III / genetics
  • Eukaryotic Cells / metabolism
  • Gene Duplication
  • Gene Fusion
  • Gene Transfer, Horizontal / genetics*
  • Genes, Bacterial / genetics*
  • Genome
  • Glycoside Hydrolases / chemistry
  • Glycoside Hydrolases / genetics
  • Host-Pathogen Interactions / genetics*
  • Molecular Sequence Data
  • Muramidase / genetics
  • N-Acetylmuramoyl-L-alanine Amidase / chemistry
  • N-Acetylmuramoyl-L-alanine Amidase / genetics
  • Polymerase Chain Reaction
  • Reproducibility of Results
  • Rickettsia / genetics

Substances

  • Bacterial Proteins
  • DNA Polymerase III
  • DNA polymerase III, alpha subunit
  • Glycoside Hydrolases
  • endo-N-acetylmuramidase
  • Muramidase
  • Carboxypeptidases
  • LD-carboxypeptidase
  • N-Acetylmuramoyl-L-alanine Amidase