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Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera.

ABSTRACT: Aphids possess bacteriocytes, cells specifically differentiated to harbor obligatory mutualistic bacteria of the genus Buchnera, which have lost many genes that are essential for common bacterial functions. To understand the host's role in maintaining the symbiotic relationship, bacteriocytes were isolated from the pea aphid, Acyrthosiphon pisum, and the host transcriptome was investigated by using EST analysis and real-time quantitative RT-PCR. A number of genes were highly expressed specifically in the bacteriocyte, including (i) genes for amino acid metabolism, including those for biosynthesis of amino acids that Buchnera cannot produce, and those for utilization of amino acids that Buchnera can synthesize; (ii) genes related to transport, including genes for mitochondrial transporters and a gene encoding Rab, a G protein that regulates vesicular transport; and (iii) genes for putative lysozymes that degrade bacterial cell walls. Significant up-regulation of i clearly indicated that the bacteriocyte is involved in the exchange of amino acids between the host aphid and Buchnera, the key metabolic process in the symbiotic system. Conspicuously high expression of ii and iii shed light on previously unknown aspects of the host-Buchnera interactions in the symbiotic system.

SUBMITTER: Nakabachi A

PROVIDER: S-EPMC555734 | biostudies-literature | 2005 Apr

REPOSITORIES: biostudies-literature

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Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera.

Nakabachi Atsushi A Shigenobu Shuji S Sakazume Naoko N Shiraki Toshiyuki T Hayashizaki Yoshihide Y Carninci Piero P Ishikawa Hajime H Kudo Toshiaki T Fukatsu Takema T

Proceedings of the National Academy of Sciences of the United States of America 20050330 15

Aphids possess bacteriocytes, cells specifically differentiated to harbor obligatory mutualistic bacteria of the genus Buchnera, which have lost many genes that are essential for common bacterial functions. To understand the host's role in maintaining the symbiotic relationship, bacteriocytes were isolated from the pea aphid, Acyrthosiphon pisum, and the host transcriptome was investigated by using EST analysis and real-time quantitative RT-PCR. A number of genes were highly expressed specifical ...[more]

PMID: 15800043

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Project description: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.

Dataset Information

Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera.

Publications

Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera.

Similar Datasets

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